Wastewater Surveillance Provides Spatiotemporal SARS-CoV-2 Infection Dynamics

Xiawan Zheng; Kathy Leung; Xiaoqing Xu; Yu Deng; Yulin Zhang; Xi Chen; Chung In Yau; Kenny W.K. Hui; Eddie Pak; Ho-Kwong Chui; Ron Yang; Hein Min Tun; Gabriel Matthew Leung; Joseph Tsz Kei Wu; Malik Peiris; Leo Lit Man Poon; Tong Zhang

doi:10.1016/j.eng.2024.01.016

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Engineering ›› 2024, Vol. 40 ›› Issue (9) : 70-77. DOI: 10.1016/j.eng.2024.01.016

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Article

Wastewater Surveillance Provides Spatiotemporal SARS-CoV-2 Infection Dynamics

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Highlights

• Large-scale intensive wastewater surveillance was conducted to obtain citywide spatiotemporal trends.

• Wastewater surveillance captured the pandemic trend three days earlier than reported cases.

• Two methods were established to estimate prevalence from wastewater datasets.

• Wastewater surveillance revealed that the reported cases were underestimated during the pandemic outbreak.

• The wastewater-based effective reproductive number (R_ww) was comparable to the incidence-based R_cc.

Abstract

Wastewater surveillance (WWS) can leverage its wide coverage, population-based sampling, and high monitoring frequency to capture citywide pandemic trends independent of clinical surveillance. Here we conducted a nine months daily WWS for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from 12 wastewater treatment plants (WWTPs), covering approximately 80% of the population, to monitor infection dynamics in Hong Kong, China. We found that the SARS-CoV-2 virus concentration in wastewater was correlated with the daily number of reported cases and reached two pandemic peaks three days earlier during the study period. In addition, two different methods were established to estimate the prevalence/incidence rates from wastewater measurements. The estimated results from wastewater were consistent with findings from two independent citywide clinical surveillance programmes (rapid antigen test (RAT) surveillance and serology surveillance), but higher than the cases number reported by the Centre for Health Protection (CHP) of Hong Kong, China. Moreover, the effective reproductive number (R_t) was estimated from wastewater measurements to reflect both citywide and regional transmission dynamics. Our findings demonstrate that large-scale intensive WWS from WWTPs provides cost-effective and timely public health information, especially when the clinical surveillance is inadequate and costly. This approach also provides insights into pandemic dynamics at higher spatiotemporal resolutions, facilitating the formulation of effective control policies and targeted resource allocation.

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Keywords

SARS-CoV-2 / Wastewater surveillance / Prevalence / Effective reproductive number

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Xiawan Zheng, Kathy Leung, Xiaoqing Xu, Yu Deng, Yulin Zhang, Xi Chen, Chung In Yau, Kenny W.K. Hui, Eddie Pak, Ho-Kwong Chui, Ron Yang, Hein Min Tun, Gabriel Matthew Leung, Joseph Tsz Kei Wu, Malik Peiris, Leo Lit Man Poon, Tong Zhang. Wastewater Surveillance Provides Spatiotemporal SARS-CoV-2 Infection Dynamics. Engineering, 2024, 40(9): 70‒77 https://doi.org/10.1016/j.eng.2024.01.016

References

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[1]	Naughton CC, Roman FA, Alvarado AGF, Tariqi AQ, Deeming MA, Bibby K, et al. Show us the data: global COVID-19 wastewater monitoring efforts, equity, and gaps. FEMS microbes 2023; 4:xtad003.

[2]	Keshaviah A, Diamond MB, Wade MJ, Scarpino SV, Ahmed W, Amman F, et al. Wastewater monitoring can anchor global disease surveillance systems. Lancet Glob Health 2023; 11(6):e976-81.

[3]	Xu X, Zheng X, Li S, Lam NS, Wang Y, Chu DKW, et al. The first case study of wastewater-based epidemiology of COVID-19 in Hong Kong. Sci Total Environ 2021; 790:148000.

[4]	Zheng X, Li S, Deng Y, Xu X, Ding J, Lau FTK, et al. Quantification of SARS-CoV-2 RNA in wastewater treatment plants mirrors the pandemic trend in Hong Kong. Sci Total Environ 2022; 844:157121.

[5]	Deng Y, Zheng X, Xu X, Chui HK, Lai WK, Li S, et al. Use of sewage surveillance for COVID-19: large-scale evidence-based program in Hong Kong. Environ Health Perspect 2022; 130(5):057008.

[6]	Deng Y, Xu X, Zheng X, Ding J, Li S, Chui HK, et al. Use of sewage surveillance for COVID-19 to guide public health response: a case study in Hong Kong. Sci Total Environ 2022; 821:153250.

[7]	Hillary LS, Farkas K, Maher KH, Lucaci A, Thorpe J, Distaso MA, et al. Monitoring SARS-CoV-2 in municipal wastewater to evaluate the success of lockdown measures for controlling COVID-19 in the UK. Water Res 2021; 200:117214.

[8]	Wu F, Xiao A, Zhang J, Moniz K, Endo N, Armas F, et al. Wastewater surveillance of SARS-CoV-2 across 40 U.S. states from February to June 2020. Water Res 2021; 202:117400.

[9]	Graham KE, Loeb SK, Wolfe MK, Catoe D, Sinnott-Armstrong N, Kim S, et al. SARS-CoV-2 RNA in wastewater settled solids is associated with COVID-19 cases in a large urban sewershed. Environ Sci Technol 2021; 55(1):488-98.

[10]	Wu F, Zhang J, Xiao A, Gu X, Lee WL, Armas F, et al. SARS-CoV-2 titers in wastewater are higher than expected from clinically confirmed cases. mSystems 2020; 5(4):e00614-20.

[11]	Jiang G, Wu J, Weidhaas J, Li X, Chen Y, Mueller J, et al. Artificial neural network-based estimation of COVID-19 case numbers and effective reproduction rate using wastewater-based epidemiology. Water Res 2022; 218:118451.

[12]	Schoen ME, Wolfe MK, Li L, Duong D, White BJ, Hughes B, et al. SARS-CoV-2 RNA wastewater settled solids surveillance frequency and impact on predicted COVID-19 incidence using a distributed lag model. ACS EST Water 2022; 2 11):2167-74.

[13]	Zulli A, Pan A, Bart SM, Crawford FW, Kaplan EH, Cartter M, et al. Predicting daily COVID-19 case rates from SARS-CoV-2 RNA concentrations across a diversity of wastewater catchments. FEMS Microbes 2021; 2:xtab022.

[14]	Huisman JS, Scire J, Caduff L, Fernandez-Cassi X, Ganesanandamoorthy P, Kull A, et al. Wastewater-based estimation of the effective reproductive number of SARS-CoV-2. Environ Health Perspect 2022; 130(5):057011.

[15]	Chow WK, Chow CL, Cheng CH. Estimation of the total number of infected cases in the 5th wave of COVID-19 in Hong Kong. 2022. medRxiv:22278708.

[16]	Zheng X, Wang M, Deng Y, Xu X, Lin D, Zhang Y, et al. A rapid, high-throughput, and sensitive PEG-precipitation method for SARS-CoV-2 wastewater surveillance. Water Res 2023; 230:119560.

[17]	Xiao A, Wu F, Bushman M, Zhang J, Imakaev M, Chai PR, et al. Metrics to relate COVID-19 wastewater data to clinical testing dynamics. Water Res 2022; 212:118070.

[18]	D’Aoust PM, Tian X, Towhid ST, Xiao A, Mercier E, Hegazy N, et al. Wastewater to clinical case (WC) ratio of COVID-19 identifies insufficient clinical testing, onset of new variants of concern and population immunity in urban communities. Sci Total Environ 2022; 853:158547.

[19]	Schmitz BW, Innes GK, Prasek SM, Betancourt WQ, Stark ER, Foster AR, et al. Enumerating asymptomatic COVID-19 cases and estimating SARS-CoV-2 fecal shedding rates via wastewater-based epidemiology. Sci Total Environ 2021; 801:149794.

[20]	Zheng S, Fan J, Yu F, Feng B, Lou B, Zou Q, et al. Viral load dynamics and disease severity in patients infected with SARS-CoV-2 in Zhejiang Province, China, January-March 2020: retrospective cohort study. BMJ 2020; 369:m1443.

[21]	Penn R, Ward BJ, Strande L, Maurer M. Review of synthetic human faeces and faecal sludge for sanitation and wastewater research. Water Res 2018; 132:222-40.

[22]	McMahan CS, Self S, Rennert L, Kalbaugh C, Kriebel D, Graves D, et al. COVID-19 wastewater epidemiology: a model to estimate infected populations. Lancet Planet Health 2021; 5(12):e874-81.

[23]	Ling Y, Xu SB, Lin YX, Tian D, Zhu ZQ, Dai FH, et al. Persistence and clearance of viral RNA in 2019 novel coronavirus disease rehabilitation patients. Chin Med J 2020; 133(9):1039-43.

[24]	Guo M, Tao W, Flavell RA, Zhu S. Potential intestinal infection and faecal-oral transmission of SARS-CoV-2. Nat Rev Gastroenterol Hepatol 2021; 18 (4):269-83.

[25]

Li Ka Shing Faculty of Medicine of The University of Hong Kong. Clarification on the interpretation of daily point prevalence of the HKU real-time community surveillance initiative [Internet]. Hong Kong: The University of Hong Kong; 2023 Jan 03 [cited 2023 May 25]. Available from: https://www.med.hku.hk/en/news/press/20230103-real-time-community-surveillanceinitiative.

[26]	Tsang NNY, So HC, Cowling BJ, Leung GM, Ip DKM. Effectiveness of BNT162b2 and CoronaVac COVID-19 vaccination against asymptomatic and symptomatic infection of SARS-CoV-2 omicron BA.2 in Hong Kong: a prospective cohort study. Lancet Infect Dis 2022; 23(4):421-34.

[27]	Lau JJ, Cheng SMS, Leung K, Lee CK, Hachim A, Tsang LCH, et al. Real-world COVID-19 vaccine effectiveness against the Omicron BA.2 variant in a SARSCoV- 2 infection-naive population. Nat Med 2023; 29(2):348-57.

[28]	Elliott P, Bodinier B, Eales O, Wang H, Haw D, Elliott J, et al. Rapid increase in Omicron infections in England during December 2021: REACT-1 study. Science 2022; 375(6587):1406-11.

[29]	Leung K, Lau EHY, Wong CKH, Leung GM, Wu JT. Estimating the transmission dynamics of SARS-CoV-2 Omicron BF.7 in Beijing after adjustment of the zero-COVID policy in November-December 2022. Nat Med 2023; 29(3):579-82.

[30]	Lin Y, Yang B, Cobey S, Lau EHY, Adam DC, Wong JY, et al. Incorporating temporal distribution of population-level viral load enables real-time estimation of COVID-19 transmission. Nat Commun 2022; 13(1):1155.

[31]	Carcereny A, Martinez-Velazquez A, Bosch A, Allende A, Truchado P, Cascales J, et al. Monitoring emergence of the SARS-CoV-2 B.1.1.7 variant through the Spanish national SARS-CoV-2 wastewater surveillance system (VATar COVID- 19). Environ Sci Technol 2021; 55(17):11756-66.

[32]	Ho J, Stange C, Suhrborg R, Wurzbacher C, Drewes JE, Tiehm A. SARS-CoV-2 wastewater surveillance in Germany: long-term RT-digital droplet PCR monitoring, suitability of primer/probe combinations and biomarker stability. Water Res 2022; 210:117977.

[33]	Agrawal S, Orschler L, Schubert S, Zachmann K, Heijnen L, Tavazzi S, et al. Prevalence and circulation patterns of SARS-CoV-2 variants in European sewage mirror clinical data of 54 European cities. Water Res 2022; 214:118162.

[34]	Medema G, Heijnen L, Elsinga G, Italiaander R, Brouwer A. Presence of SARScoronavirus- 2 RNA in sewage and correlation with reported COVID-19 prevalence in the early stage of the epidemic in the Netherlands. Environ Sci Technol Lett 2020; 7(7):511-6.

[35]

The Government of the Hong Kong Special Administrative Region. Government announces adjustments to quarantine arrangements for inbound persons [internet]. Hong Kong: The Government of the Hong Kong Special Administrative Region; 2022 Aug 08 [cited 2023 May 25]. Available from: https://www.info.gov.hk/gia/general/202208/08/P2022080800803.htm.

[36]

The Government of the Hong Kong Special Administrative Region. Government announces lifting of compulsory quarantine requirement on arrival at Hong Kong [internet]. Hong Kong: The Government of the Hong Kong Special Administrative Region; 2022 Sep 24 [cited 2023 May 25]. Available from: https://www.info.gov.hk/gia/general/202209/24/P2022092400048.htm.

[37]	Flacco ME, Acuti Martellucci C, Baccolini V, De Vito C, Renzi E, Villari P, et al. Risk of reinfection and disease after SARS-CoV-2 primary infection: metaanalysis. Eur J Clin Invest 2022; 52(10):e13845.