Medical diagnostic tests to detect Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2) for individuals in the United States were initially limited to people who were traveling or symptomatic to track disease incidence due to the cost of providing testing for all people in a community on a routine basis. As an alternative to randomly sampling large groups of people to track disease incidence at significant cost, wastewater-based epidemiology (WBE) is a well-established and cost-effective technique to passively measure the prevalence of disease in communities without requiring invasive testing. WBE can also be used as a forecasting tool since the virus is shed in individuals prior to developing symptoms that might otherwise prompt testing. This study applied the WBE approach to understand its effectiveness as a possible forecasting tool by monitoring the SARS-CoV-2 levels in raw wastewater sampled from sewer lift stations at a large public university campus setting including dormitories, academic buildings, and athletic facilities. The WBE analysis was conducted by sampling from building-specific lift stations and enumerating target viral copies using RT-qPCR analysis. The WBE results were compared with the 7-day rolling averages of confirmed infected individuals for the following week after the wastewater sample analysis. In most cases, changes in the WBE outcomes were followed by similar trends in the clinical data. The positive predictive value of the applied WBE approach was 86% for the following week of the sample collection. In contrast, positive correlations between the two data with Spearmen correlation (rs) ranged from 0.16 to 0.36. A stronger correlation (rs = 0.18 to 0.51) was observed when WBE results were compared with COVID-19 cases identified on the next day of the sampling events. The P value of 0.007 for Dorm A suggests high significance, while moderate significance was observed for the other dormitories (B, C, and D). The outcomes of this investigation demonstrate that WBE can be a valuable tool to track the progression of diseases like COVID-19 seven days before diagnostic cases are confirmed, allowing authorities to take necessary measures in advance and also enable authorities to decide to reopen a facility after a quarantine.
References
[1]
Ahmed, W., Bertsch, P.M., Bibby, K., Haramoto, E., Hewitt, J., Huygens, F., et al. (2020) Decay of SARS-CoV-2 and Surrogate Murine Hepatitis Virus RNA in Untreated Wastewater to Inform Application in Wastewater-Based Epidemiology. Environmental Research, 191, Article 110092. https://doi.org/10.1016/j.envres.2020.110092
[2]
Ahmed, W., Angel, N., Edson, J., Bibby, K., Bivins, A., O’Brien, J.W., et al. (2020) First Confirmed Detection of SARS-CoV-2 in Untreated Wastewater in Australia: A Proof of Concept for the Wastewater Surveillance of COVID-19 in the Community. Science of the Total Environment, 728, Article 138764. https://doi.org/10.1016/j.scitotenv.2020.138764
[3]
Gonzalez, R., Curtis, K., Bivins, A., Bibby, K., Weir, M.H., Yetka, K., et al. (2020) COVID-19 Surveillance in Southeastern Virginia Using Wastewater-Based Epidemiology. Water Research, 186, Article 116296. https://doi.org/10.1016/j.watres.2020.116296
[4]
Center for Diseases Control and Prevention (CDC) (2020) How COVID-19 Spreads. https://www.cdc.gov/coronavirus/2019-ncov/prevent-getting-sick/how-COVID-spreads.html
[5]
Center for Diseases Control and Prevention (CDC) (2020) Symptoms of Coronavirus. https://www.cdc.gov/coronavirus/2019-ncov/symptoms-testing/symptoms.html
[6]
Alimohamadi, Y., Sepandi, M., Taghdir, M. and Hosamirudsari, H. (2020) Determine the Most Common Clinical Symptoms in COVID-19 Patients: A Systematic Review and Meta-Analysis. Journal of Preventive Medicine and Hygiene, 61, E304-E312. https://doi.org/10.15167/2421-4248/jpmh2020.61.3.1530
[7]
Polo, D., Quintela-Baluja, M., Corbishley, A., Jones, D.L., Singer, A.C., Graham, D.W., et al. (2020) Making Waves: Wastewater-Based Epidemiology for COVID-19—Approaches and Challenges for Surveillance and Prediction. Water Research, 186, Article 116404. https://doi.org/10.1016/j.watres.2020.116404
[8]
Mizumoto, K., Kagaya, K., Zarebski, A. and Chowell, G. (2020) Estimating the Asymptomatic Proportion of Coronavirus Disease 2019 (COVID-19) Cases on Board the Diamond Princess Cruise Ship, Yokohama, Japan, 2020. Eurosurveillance, 25, Article 2000180. https://doi.org/10.2807/1560-7917.es.2020.25.10.2000180
[9]
Wang, X.W., Li, J., Guo, T., Zhen, B., Kong, Q., Yi, B., et al. (2005) Concentration and Detection of SARS Coronavirus in Sewage from Xiao Tang Shan Hospital and the 309th Hospital of the Chinese People’s Liberation Army. Water Science and Technology, 52, 213-221. https://doi.org/10.2166/wst.2005.0266
[10]
Hart, O.E. and Halden, R.U. (2020) Computational Analysis of SARS-CoV-2/COVID-19 Surveillance by Wastewater-Based Epidemiology Locally and Globally: Feasibility, Economy, Opportunities and Challenges. Science of the Total Environment, 730, Article 138875. https://doi.org/10.1016/j.scitotenv.2020.138875
[11]
Daughton, C.G. (2001) Pharmaceuticals and Personal Care Products in the Environment: Overarching Issues and Overview. ACS Symposium Series, 791, 2-38. https://doi.org/10.1021/bk-2001-0791.ch001
[12]
Zuccato, E., Chiabrando, C., Castiglioni, S., Calamari, D., Bagnati, R., Schiarea, S., et al. (2005) Cocaine in Surface Waters: A New Evidence-Based Tool to Monitor Community Drug Abuse. Environmental Health, 4, Article No. 14. https://doi.org/10.1186/1476-069x-4-14
[13]
Leknes, H., Sturtzel, I.E. and Dye, C. (2012) Environmental Release of Oseltamivir from a Norwegian Sewage Treatment Plant during the 2009 Influenza a (H1N1) Pandemic. Science of the Total Environment, 414, 632-638. https://doi.org/10.1016/j.scitotenv.2011.11.004
[14]
Takanami, R., Ozaki, H., Giri, R.R., Taniguchi, S. and Hayashi, S. (2012) Antiviral Drugs Zanamivir and Oseltamivir Found in Wastewater and Surface Water in Osaka, Japan. Journal of Water and Environment Technology, 10, 57-68. https://doi.org/10.2965/jwet.2012.57
[15]
Sims, N. and Kasprzyk-Hordern, B. (2020) Future Perspectives of Wastewater-Based Epidemiology: Monitoring Infectious Disease Spread and Resistance to the Community Level. Environment International, 139, Article 105689. https://doi.org/10.1016/j.envint.2020.105689
[16]
Reid, M.J., Langford, K.H., Mørland, J. and Thomas, K.V. (2011) Analysis and Interpretation of Specific Ethanol Metabolites, Ethyl Sulfate, and Ethyl Glucuronide in Sewage Effluent for the Quantitative Measurement of Regional Alcohol Consumption. Alcoholism: Clinical and Experimental Research, 35, 1593-1599. https://doi.org/10.1111/j.1530-0277.2011.01505.x
[17]
Kinyua, J., Covaci, A., Maho, W., McCall, A., Neels, H. and van Nuijs, A.L.N. (2015) Sewage‐Based Epidemiology in Monitoring the Use of New Psychoactive Substances: Validation and Application of an Analytical Method Using LC‐MS/MS. Drug Testing and Analysis, 7, 812-818. https://doi.org/10.1002/dta.1777
[18]
Reid, M.J., Derry, L. and Thomas, K.V. (2013) Analysis of New Classes of Recreational Drugs in Sewage: Synthetic Cannabinoids and Amphetamine‐Like Substances. Drug Testing and Analysis, 6, 72-79. https://doi.org/10.1002/dta.1461
[19]
Sims, N., Rice, J. and Kasprzyk-Hordern, B. (2019) An Ultra-High-Performance Liquid Chromatography Tandem Mass Spectrometry Method for Oxidative Stress Biomarker Analysis in Wastewater. Analytical and Bioanalytical Chemistry, 411, 2261-2271. https://doi.org/10.1007/s00216-019-01667-8
[20]
Ryu, Y., Reid, M.J. and Thomas, K.V. (2015) Liquid Chromatography-High Resolution Mass Spectrometry with Immunoaffinity Clean-up for the Determination of the Oxidative Stress Biomarker 8-Iso-Prostaglandin F2alpha in Wastewater. Journal of Chromatography A, 1409, 146-151. https://doi.org/10.1016/j.chroma.2015.07.060
[21]
Been, F., Bastiaensen, M., Lai, F.Y., van Nuijs, A.L.N. and Covaci, A. (2017) Liquid Chromatography-Tandem Mass Spectrometry Analysis of Biomarkers of Exposure to Phosphorus Flame Retardants in Wastewater to Monitor Community-Wide Exposure. Analytical Chemistry, 89, 10045-10053. https://doi.org/10.1021/acs.analchem.7b02705
[22]
Lopardo, L., Petrie, B., Proctor, K., Youdan, J., Barden, R. and Kasprzyk-Hordern, B. (2019) Estimation of Community-Wide Exposure to Bisphenol a via Water Fingerprinting. Environment International, 125, 1-8. https://doi.org/10.1016/j.envint.2018.12.048
[23]
Testai, E., Galli, C.L., Dekant, W., Marinovich, M., Piersma, A.H. and Sharpe, R.M. (2013) A Plea for Risk Assessment of Endocrine Disrupting Chemicals. Toxicology, 314, 51-59. https://doi.org/10.1016/j.tox.2013.07.018
[24]
Lai, F.Y., Been, F., Covaci, A. and van Nuijs, A.L.N. (2017) Novel Wastewater-Based Epidemiology Approach Based on Liquid Chromatography-Tandem Mass Spectrometry for Assessing Population Exposure to Tobacco-Specific Toxicants and Carcinogens. Analytical Chemistry, 89, 9268-9278. https://doi.org/10.1021/acs.analchem.7b02052
[25]
Gracia-Lor, E., Zuccato, E., Hernández, F. and Castiglioni, S. (2020) Wastewater-Based Epidemiology for Tracking Human Exposure to Mycotoxins. Journal of Hazardous Materials, 382, Article 121108. https://doi.org/10.1016/j.jhazmat.2019.121108
[26]
Shannon, K.E., Lee, D.-Y., Trevors, J.T. and Beaudette, L.A. (2007) Application of Real-Time Quantitative PCR for the Detection of Selected Bacterial Pathogens during Municipal Wastewater Treatment. Science of the Total Environment, 382, 121-129. https://doi.org/10.1016/j.scitotenv.2007.02.039
[27]
Hellmér, M., Paxéus, N., Magnius, L., Enache, L., Arnholm, B., Johansson, A., et al. (2014) Detection of Pathogenic Viruses in Sewage Provided Early Warnings of Hepatitis a Virus and Norovirus Outbreaks. Applied and Environmental Microbiology, 80, 6771-6781. https://doi.org/10.1128/aem.01981-14
[28]
Heijnen, L. and Medema, G. (2011) Surveillance of Influenza A and the Pandemic Influenza A (H1N1) 2009 in Sewage and Surface Water in the Netherlands. Journal of Water and Health, 9, 434-442. https://doi.org/10.2166/wh.2011.019
[29]
Gourinat, A., O’Connor, O., Calvez, E., Goarant, C. and Dupont-Rouzeyrol, M. (2015) Detection of Zika Virus in Urine. Emerging Infectious Diseases, 21, 84-86.
[30]
Poloni, T.R., Oliveira, A.S., Alfonso, H.L., Galvão, L.R., Amarilla, A.A., Poloni, D.F., et al. (2010) Detection of Dengue Virus in Saliva and Urine by Real Time RT-PCR. Virology Journal, 7, Article No. 22. https://doi.org/10.1186/1743-422x-7-22
[31]
Poon, L.L.M., Chan, K.H., Wong, O.K., Cheung, T.K.W., Ng, I., Zheng, B., et al. (2004) Detection of SARS Coronavirus in Patients with Severe Acute Respiratory Syndrome by Conventional and Real-Time Quantitative Reverse Transcription-PCR Assays. Clinical Chemistry, 50, 67-72. https://doi.org/10.1373/clinchem.2003.023663
[32]
Street, R., Malema, S., Mahlangeni, N. and Mathee, A. (2020) Wastewater Surveillance for COVID-19: An African Perspective. Science of the Total Environment, 743, Article 140719. https://doi.org/10.1016/j.scitotenv.2020.140719
[33]
Daughton, C.G. (2020) Wastewater Surveillance for Population-Wide COVID-19: The Present and Future. Science of the Total Environment, 736, Article 139631. https://doi.org/10.1016/j.scitotenv.2020.139631
[34]
Ort, C., Banta-Green, C.J., Bijlsma, L., Castiglioni, S., Emke, E., Gartner, C., et al. (2014) Sewage-Based Epidemiology Requires a Truly Transdisciplinary Approach. GAIA-Ecological Perspectives for Science and Society, 23, 266-268. https://doi.org/10.14512/gaia.23.3.12
[35]
Orive, G., Lertxundi, U. and Barcelo, D. (2020) Early SARS-CoV-2 Outbreak Detection by Sewage-Based Epidemiology. Science of the Total Environment, 732, Article 139298. https://doi.org/10.1016/j.scitotenv.2020.139298
[36]
Zhou, R., Li, F., Chen, F., Liu, H., Zheng, J., Lei, C., et al. (2020) Viral Dynamics in Asymptomatic Patients with COVID-19. International Journal of Infectious Diseases, 96, 288-290. https://doi.org/10.1016/j.ijid.2020.05.030
[37]
Badu, K., Oyebola, K., Zahouli, J.Z.B., Fagbamigbe, A.F., de Souza, D.K., Dukhi, N., et al. (2021) SARS-CoV-2 Viral Shedding and Transmission Dynamics: Implications of WHO COVID-19 Discharge Guidelines. Frontiers in Medicine, 8, Article 648660. https://doi.org/10.3389/fmed.2021.648660
[38]
He, X., Lau, E.H.Y., Wu, P., Deng, X., Wang, J., Hao, X., et al. (2020) Temporal Dynamics in Viral Shedding and Transmissibility of COVID-19. Nature Medicine, 26, 672-675. https://doi.org/10.1038/s41591-020-0869-5
[39]
Cevik, M., Tate, M., Lloyd, O., Maraolo, A.E., Schafers, J. and Ho, A. (2021) SARS-CoV-2, SARS-CoV, and MERS-CoV Viral Load Dynamics, Duration of Viral Shedding, and Infectiousness: A Systematic Review and Meta-Analysis. The Lancet Microbe, 2, E13-E22. https://doi.org/10.1016/s2666-5247(20)30172-5
[40]
Puhach, O., Meyer, B. and Eckerle, I. (2022) SARS-CoV-2 Viral Load and Shedding Kinetics. Nature Reviews Microbiology, 21, 147-161. https://doi.org/10.1038/s41579-022-00822-w
[41]
Peccia, J., Zulli, A., Brackney, D.E., Grubaugh, N.D., Kaplan, E.H., Casanovas-Massana, A., et al. (2020) Measurement of SARS-CoV-2 RNA in Wastewater Tracks Community Infection Dynamics. Nature Biotechnology, 38, 1164-1167. https://doi.org/10.1038/s41587-020-0684-z
[42]
Aguiar-Oliveira, M.L., Campos, A., R. Matos, A., Rigotto, C., Sotero-Martins, A., Teixeira, P.F.P., et al. (2020) Wastewater-Based Epidemiology (WBE) and Viral Detection in Polluted Surface Water: A Valuable Tool for COVID-19 Surveillance—A Brief Review. International Journal of Environmental Research and Public Health, 17, Article 9251. https://doi.org/10.3390/ijerph17249251
[43]
Grube, A.M., Coleman, C.K., LaMontagne, C.D., Miller, M.E., Kothegal, N.P., Holcomb, D.A., et al. (2023) Detection of SARS-CoV-2 RNA in Wastewater and Comparison to COVID-19 Cases in Two Sewersheds, North Carolina, USA. Science of the Total Environment, 858, Article 159996. https://doi.org/10.1016/j.scitotenv.2022.159996
[44]
Kim, L.H., Mikolaityte, V. and Kim, S. (2023) Establishment of Wastewater-Based SARS-CoV-2 Monitoring System Over Two Years: Case Studies in South Korea. Journal of Environmental Chemical Engineering, 11, Article 110289. https://doi.org/10.1016/j.jece.2023.110289
[45]
Rothman, J.A., Loveless, T.B., Kapcia, J., Adams, E.D., Steele, J.A., Zimmer-Faust, A.G., et al. (2021) RNA Viromics of Southern California Wastewater and Detection of SARS-CoV-2 Single-Nucleotide Variants. Applied and Environmental Microbiology, 87, e01448-21. https://doi.org/10.1128/aem.01448-21
[46]
Lu, D., Huang, Z., Luo, J., Zhang, X. and Sha, S. (2020) Primary Concentration—The Critical Step in Implementing the Wastewater Based Epidemiology for the COVID-19 Pandemic: A Mini-Review. Science of the Total Environment, 747, Article 141245. https://doi.org/10.1016/j.scitotenv.2020.141245
[47]
Holshue, M.L., DeBolt, C., Lindquist, S., Lofy, K.H., Wiesman, J., Bruce, H., et al. (2020) First Case of 2019 Novel Coronavirus in the United States. New England Journal of Medicine, 382, 929-936. https://doi.org/10.1056/nejmoa2001191
[48]
Tang, A., Tong, Z., Wang, H., Dai, Y., Li, K., Liu, J., et al. (2020) Detection of Novel Coronavirus by RT-PCR in Stool Specimen from Asymptomatic Child, China. Emerging Infectious Diseases, 26, 1337-1339.
[49]
Xiao, F., Tang, M., Zheng, X., Liu, Y., Li, X. and Shan, H. (2020) Evidence for Gastrointestinal Infection of SARS-CoV-2. Gastroenterology, 158, 1831-1833.E3. https://doi.org/10.1053/j.gastro.2020.02.055
[50]
Haramoto, E., Malla, B., Thakali, O. and Kitajima, M. (2020) First Environmental Surveillance for the Presence of SARS-CoV-2 RNA in Wastewater and River Water in Japan. Science of the Total Environment, 737, 140405. https://doi.org/10.1016/j.scitotenv.2020.140405
[51]
Sherchan, S.P., Shahin, S., Ward, L.M., Tandukar, S., Aw, T.G., Schmitz, B., et al. (2020) First Detection of SARS-CoV-2 RNA in Wastewater in North America: A Study in Louisiana, USA. Science of the Total Environment, 743, Article 140621. https://doi.org/10.1016/j.scitotenv.2020.140621
[52]
Arora, S., Nag, A., Sethi, J., Rajvanshi, J., Saxena, S., Shrivastava, S.K., et al. (2020) Sewage Surveillance for the Presence of SARS-CoV-2 Genome as a Useful Wastewater Based Epidemiology (WBE) Tracking Tool in India. Water Science and Technology, 82, 2823-2836. https://doi.org/10.2166/wst.2020.540
[53]
Hasan, S.W., Ibrahim, Y., Daou, M., Kannout, H., Jan, N., et al. (2020) Detection and Quantification of SARS-CoV-2 RNA in Wastewater and Treated Effluents: Surveillance of COVID-19 Epidemic in the United Arab Emirates. Science of the Total Environment, 764, Article 142929. https://doi.org/10.1016/j.scitotenv.2020.142929
[54]
Albastaki, A., Naji, M., Lootah, R., Almeheiri, R., Almulla, H., Almarri, I., et al. (2021) First Confirmed Detection of SARS-CoV-2 in Untreated Municipal and Aircraft Wastewater in Dubai, UAE: The Use of Wastewater Based Epidemiology as an Early Warning Tool to Monitor the Prevalence of COVID-19. Science of the Total Environment, 760, Article 143350. https://doi.org/10.1016/j.scitotenv.2020.143350
[55]
McMahan, C.S., Self, S., Rennert, L., Kalbaugh, C., Kriebel, D., Graves, D., et al. (2020) COVID-19 Wastewater Epidemiology: A Model to Estimate Infected Populations. The Lancet Planetary Health, 5, E874-E881. https://doi.org/10.1016/S2542-5196(21)00230-8
[56]
Bivins, A., Greaves, J., Fischer, R., Yinda, K.C., Ahmed, W., Kitajima, M., et al. (2020) Persistence of SARS-CoV-2 in Water and Wastewater. Environmental Science & Technology Letters, 7, 937-942. https://doi.org/10.1021/acs.estlett.0c00730
[57]
Kumar, M., Patel, A.K., Shah, A.V., Raval, J., Rajpara, N., Joshi, M., et al. (2020) First Proof of the Capability of Wastewater Surveillance for COVID-19 in India through Detection of Genetic Material of SARS-CoV-2. Science of the Total Environment, 746, Article 141326. https://doi.org/10.1016/j.scitotenv.2020.141326
[58]
Medema, G., Heijnen, L., Elsinga, G., Italiaander, R. and Brouwer, A. (2020) Presence of SARS-Coronavirus-2 RNA in Sewage and Correlation with Reported COVID-19 Prevalence in the Early Stage of the Epidemic in the Netherlands. Environmental Science & Technology Letters, 7, 511-516. https://doi.org/10.1021/acs.estlett.0c00357
[59]
Wurtzer, S., Marechal, V., Mouchel, J.M., Maday, Y., Teyssou, R., Richard, E., et al. (2020) Evaluation of Lockdown Impact on SARS-CoV-2 Dynamics through Viral Genome Quantification in Paris Wastewaters. Eurosurveillance, 25, Article ID: 2000776. https://doi.org/10.2807/1560-7917.es.2020.25.50.2000776
[60]
Galani, A., Aalizadeh, R., Kostakis, M., Markou, A., Alygizakis, N., Lytras, T., et al. (2022) SARS-CoV-2 Wastewater Surveillance Data Can Predict Hospitalizations and ICU Admissions. Science of the Total Environment, 804, Article 150151. https://doi.org/10.1016/j.scitotenv.2021.150151
[61]
Randazzo, W., Truchado, P., Cuevas-Ferrando, E., Simón, P., Allende, A. and Sánchez, G. (2020) SARS-CoV-2 RNA in Wastewater Anticipated COVID-19 Occurrence in a Low Prevalence Area. Water Research, 181, Article 115942. https://doi.org/10.1016/j.watres.2020.115942
[62]
Betancourt, W.Q., Schmitz, B.W., Innes, G.K., Prasek, S.M., Pogreba Brown, K.M., Stark, E.R., et al. (2021) COVID-19 Containment on a College Campus via Wastewater-Based Epidemiology, Targeted Clinical Testing and an Intervention. Science of the Total Environment, 779, Article 146408. https://doi.org/10.1016/j.scitotenv.2021.146408
[63]
Sharara, N., Endo, N., Duvallet, C., Ghaeli, N., Matus, M., Heussner, J., et al. (2021) Wastewater Network Infrastructure in Public Health: Applications and Learnings from the COVID-19 Pandemic. PLOS Global Public Health, 1, e0000061. https://doi.org/10.1371/journal.pgph.0000061
[64]
Colombet, J., Robin, A., Lavie, L., Bettarel, Y., Cauchie, H.M. and Sime-Ngando, T. (2007) Virioplankton ‘Pegylation’: Use of PEG (Polyethylene Glycol) to Concentrate and Purify Viruses in Pelagic Ecosystems. Journal of Microbiological Methods, 71, 212-219. https://doi.org/10.1016/j.mimet.2007.08.012
[65]
USA Facts (2022) Palm Beach County, Florida Coronavirus Cases and Deaths. https://usafacts.org/visualizations/coronavirus-covid-19-spread-map/state/florida/county/palm-beach-county/
[66]
Zhan, Q., Babler, K.M., Sharkey, M.E., Amirali, A., Beaver, C.C., Boone, M.M., et al. (2022) Relationships between SARS-CoV-2 in Wastewater and COVID-19 Clinical Cases and Hospitalizations, with and without Normalization against Indicators of Human Waste. ACS ES&T Water, 2, 1992-2003. https://doi.org/10.1021/acsestwater.2c00045
