COVID-19 monitoring with sparse sampling of sewered and non-sewered wastewater in urban and rural communities

doi:10.1016/j.isci.2023.107019

. 2023 Jul 21;26(7):107019.

doi: 10.1016/j.isci.2023.107019. Epub 2023 Jun 9.

COVID-19 monitoring with sparse sampling of sewered and non-sewered wastewater in urban and rural communities

Dhammika Leshan Wannigama^{1

2

3

4

5

6}, Mohan Amarasiri⁷, Parichart Hongsing^{8

9}, Cameron Hurst^{10

11}, Charin Modchang^{12

13

14}, Sudarat Chadsuthi¹⁵, Suparinthon Anupong¹², Phatthranit Phattharapornjaroen^{16

17}, Ali Hosseini Rad S M^{18

19}, Stefan Fernandez²⁰, Angkana T Huang²⁰, Porames Vatanaprasan¹⁶, Dylan John Jay⁶, Thammakorn Saethang²¹, Sirirat Luk-In²², Robin James Storer²³, Puey Ounjai²⁴, Naveen Kumar Devanga Ragupathi^{4

25

26}, Phitsanuruk Kanthawee²⁷, Daisuke Sano^{28

29}, Takashi Furukawa⁷, Kazunari Sei⁷, Asada Leelahavanichkul^{1

30}, Talerngsak Kanjanabuch^{31

32

33

34}, Nattiya Hirankarn^{2

19}, Paul G Higgins^{35

36}, Anthony Kicic^{37

38

39

40}, Andrew C Singer⁴¹, Tanittha Chatsuwan^{2

3}, Sam Trowsdale⁴², Shuichi Abe¹, Alexander D McLellan¹⁸, Hitoshi Ishikawa⁴³

Affiliations

¹ Department of Infectious Diseases and Infection Control, Yamagata Prefectural Central Hospital, Yamagata, Japan.
² Department of Microbiology, Faculty of Medicine, Chulalongkorn University, King Chulalongkorn Memorial Hospital, Thai Red Cross Society, Bangkok, Thailand.
³ Center of Excellence in Antimicrobial Resistance and Stewardship, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
⁴ School of Medicine, Faculty of Health and Medical Sciences, The University of Western Australia, Nedlands, WA, Australia.
⁵ Biofilms and Antimicrobial Resistance Consortium of ODA receiving countries, The University of Sheffield, Sheffield, UK.
⁶ Pathogen Hunter's Research Collaborative Team, Department of Infectious Diseases and Infection Control, Yamagata Prefectural Central Hospital, Yamagata, Japan.
⁷ Laboratory of Environmental Hygiene, Department of Health Science, School of Allied Health Sciences, Graduate School of Medical Sciences, Kitasato University, Kitasato, Sagamihara-Minami, Kanagawa 252-0373, Japan.
⁸ Mae Fah Luang University Hospital, Chiang Rai, Thailand.
⁹ School of Integrative Medicine, Mae Fah Luang University, Chiang Rai, Thailand.
¹⁰ Molly Wardaguga Research Centre, Charles Darwin University, Brisbane, QLD, Australia.
¹¹ Statistics, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia.
¹² Biophysics Group, Department of Physics, Faculty of Science, Mahidol University, Bangkok 10400, Thailand.
¹³ Centre of Excellence in Mathematics, MHESI, Bangkok 10400, Thailand.
¹⁴ Thailand Center of Excellence in Physics, Ministry of Higher Education, Science, Research and Innovation, 328 Si Ayutthaya Road, Bangkok 10400, Thailand.
¹⁵ Department of Physics, Faculty of Science, Naresuan University, Phitsanulok 65000, Thailand.
¹⁶ Faculty of Medicine Ramathibodi Hospital, Mahidol University, Bangkok, Thailand.
¹⁷ Institute of Clinical Sciences, Department of Surgery, Sahlgrenska Academy, Gothenburg University, 40530 Gothenburg, Sweden.
¹⁸ Department of Microbiology and Immunology, University of Otago, Dunedin, Otago 9010, New Zealand.
¹⁹ Center of Excellence in Immunology and Immune-Mediated Diseases, Chulalongkorn University, Bangkok 10330, Thailand.
²⁰ Department of Virology, U.S. Army Medical Directorate, Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand.
²¹ Department of Computer Science, Faculty of Science, Kasetsart University, Bangkok, Thailand.
²² Department of Clinical Microbiology and Applied Technology, Faculty of Medical Technology, Mahidol University, Bangkok, Thailand.
²³ Office of Research Affairs, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
²⁴ Department of Biology, Faculty of Science, Mahidol University, Bangkok, Thailand.
²⁵ Department of Chemical and Biological Engineering, The University of Sheffield, Sheffield, UK.
²⁶ Department of Clinical Microbiology, Christian Medical College, Vellore, India.
²⁷ Public Health major, School of Health Science, Mae Fah Luang University, Chiang Rai, Thailand.
²⁸ Department of Frontier Sciences for Advanced Environment, Graduate School of Environmental Studies, Tohoku University, Sendai, Miyagi, Japan.
²⁹ Department of Civil and Environmental Engineering, Graduate School of Engineering, Tohoku University, Sendai, Miyagi, Japan.
³⁰ Translational Research in Inflammation and Immunology Research Unit (TRIRU), Department of Microbiology, Chulalongkorn University, Bangkok, Thailand.
³¹ Division of Nephrology, Department of Medicine, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
³² Center of Excellence in Kidney Metabolic Disorders, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
³³ Dialysis Policy and Practice Program (DiP3), School of Global Health, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
³⁴ Peritoneal Dialysis Excellence Center, King Chulalongkorn Memorial Hospital, Bangkok, Thailand.
³⁵ Institute for Medical Microbiology, Immunology and Hygiene, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
³⁶ German Centre for Infection Research, Partner site Bonn-Cologne, Cologne, Germany.
³⁷ Wal-Yan Respiratory Research Centre, Telethon Kids Institute, University of Western Australia, Nedlands, WA 6009, Australia.
³⁸ Centre for Cell Therapy and Regenerative Medicine, Medical School, The University of Western Australia, Nedlands, WA 6009, Australia.
³⁹ Department of Respiratory and Sleep Medicine, Perth Children's Hospital, Nedlands, WA 6009, Australia.
⁴⁰ School of Population Health, Curtin University, Bentley, WA 6102, Australia.
⁴¹ UK Centre for Ecology & Hydrology, OX10 8BB Wallingford, UK.
⁴² Department of Environmental Science, University of Auckland, Auckland 1010, New Zealand.
⁴³ Yamagata Prefectural University of Health Sciences, Kamiyanagi, Yamagata 990-2212, Japan.

PMID: 37351501
PMCID: PMC10250052
DOI: 10.1016/j.isci.2023.107019

COVID-19 monitoring with sparse sampling of sewered and non-sewered wastewater in urban and rural communities

Dhammika Leshan Wannigama et al. iScience. 2023.

. 2023 Jul 21;26(7):107019.

doi: 10.1016/j.isci.2023.107019. Epub 2023 Jun 9.

Authors

Affiliations

¹ Department of Infectious Diseases and Infection Control, Yamagata Prefectural Central Hospital, Yamagata, Japan.
² Department of Microbiology, Faculty of Medicine, Chulalongkorn University, King Chulalongkorn Memorial Hospital, Thai Red Cross Society, Bangkok, Thailand.
³ Center of Excellence in Antimicrobial Resistance and Stewardship, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
⁴ School of Medicine, Faculty of Health and Medical Sciences, The University of Western Australia, Nedlands, WA, Australia.
⁵ Biofilms and Antimicrobial Resistance Consortium of ODA receiving countries, The University of Sheffield, Sheffield, UK.
⁶ Pathogen Hunter's Research Collaborative Team, Department of Infectious Diseases and Infection Control, Yamagata Prefectural Central Hospital, Yamagata, Japan.
⁷ Laboratory of Environmental Hygiene, Department of Health Science, School of Allied Health Sciences, Graduate School of Medical Sciences, Kitasato University, Kitasato, Sagamihara-Minami, Kanagawa 252-0373, Japan.
⁸ Mae Fah Luang University Hospital, Chiang Rai, Thailand.
⁹ School of Integrative Medicine, Mae Fah Luang University, Chiang Rai, Thailand.
¹⁰ Molly Wardaguga Research Centre, Charles Darwin University, Brisbane, QLD, Australia.
¹¹ Statistics, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia.
¹² Biophysics Group, Department of Physics, Faculty of Science, Mahidol University, Bangkok 10400, Thailand.
¹³ Centre of Excellence in Mathematics, MHESI, Bangkok 10400, Thailand.
¹⁴ Thailand Center of Excellence in Physics, Ministry of Higher Education, Science, Research and Innovation, 328 Si Ayutthaya Road, Bangkok 10400, Thailand.
¹⁵ Department of Physics, Faculty of Science, Naresuan University, Phitsanulok 65000, Thailand.
¹⁶ Faculty of Medicine Ramathibodi Hospital, Mahidol University, Bangkok, Thailand.
¹⁷ Institute of Clinical Sciences, Department of Surgery, Sahlgrenska Academy, Gothenburg University, 40530 Gothenburg, Sweden.
¹⁸ Department of Microbiology and Immunology, University of Otago, Dunedin, Otago 9010, New Zealand.
¹⁹ Center of Excellence in Immunology and Immune-Mediated Diseases, Chulalongkorn University, Bangkok 10330, Thailand.
²⁰ Department of Virology, U.S. Army Medical Directorate, Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand.
²¹ Department of Computer Science, Faculty of Science, Kasetsart University, Bangkok, Thailand.
²² Department of Clinical Microbiology and Applied Technology, Faculty of Medical Technology, Mahidol University, Bangkok, Thailand.
²³ Office of Research Affairs, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
²⁴ Department of Biology, Faculty of Science, Mahidol University, Bangkok, Thailand.
²⁵ Department of Chemical and Biological Engineering, The University of Sheffield, Sheffield, UK.
²⁶ Department of Clinical Microbiology, Christian Medical College, Vellore, India.
²⁷ Public Health major, School of Health Science, Mae Fah Luang University, Chiang Rai, Thailand.
²⁸ Department of Frontier Sciences for Advanced Environment, Graduate School of Environmental Studies, Tohoku University, Sendai, Miyagi, Japan.
²⁹ Department of Civil and Environmental Engineering, Graduate School of Engineering, Tohoku University, Sendai, Miyagi, Japan.
³⁰ Translational Research in Inflammation and Immunology Research Unit (TRIRU), Department of Microbiology, Chulalongkorn University, Bangkok, Thailand.
³¹ Division of Nephrology, Department of Medicine, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
³² Center of Excellence in Kidney Metabolic Disorders, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
³³ Dialysis Policy and Practice Program (DiP3), School of Global Health, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.
³⁴ Peritoneal Dialysis Excellence Center, King Chulalongkorn Memorial Hospital, Bangkok, Thailand.
³⁵ Institute for Medical Microbiology, Immunology and Hygiene, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
³⁶ German Centre for Infection Research, Partner site Bonn-Cologne, Cologne, Germany.
³⁷ Wal-Yan Respiratory Research Centre, Telethon Kids Institute, University of Western Australia, Nedlands, WA 6009, Australia.
³⁸ Centre for Cell Therapy and Regenerative Medicine, Medical School, The University of Western Australia, Nedlands, WA 6009, Australia.
³⁹ Department of Respiratory and Sleep Medicine, Perth Children's Hospital, Nedlands, WA 6009, Australia.
⁴⁰ School of Population Health, Curtin University, Bentley, WA 6102, Australia.
⁴¹ UK Centre for Ecology & Hydrology, OX10 8BB Wallingford, UK.
⁴² Department of Environmental Science, University of Auckland, Auckland 1010, New Zealand.
⁴³ Yamagata Prefectural University of Health Sciences, Kamiyanagi, Yamagata 990-2212, Japan.

PMID: 37351501
PMCID: PMC10250052
DOI: 10.1016/j.isci.2023.107019

Abstract

Equitable SARS-CoV-2 surveillance in low-resource communities lacking centralized sewers is critical as wastewater-based epidemiology (WBE) progresses. However, large-scale studies on SARS-CoV-2 detection in wastewater from low-and middle-income countries is limited because of economic and technical reasons. In this study, wastewater samples were collected twice a month from 186 urban and rural subdistricts in nine provinces of Thailand mostly having decentralized and non-sewered sanitation infrastructure and analyzed for SARS-CoV-2 RNA variants using allele-specific RT-qPCR. Wastewater SARS-CoV-2 RNA concentration was used to estimate the real-time incidence and time-varying effective reproduction number (R_e). Results showed an increase in SARS-CoV-2 RNA concentrations in wastewater from urban and rural areas 14-20 days earlier than infected individuals were officially reported. It also showed that community/food markets were "hot spots" for infected people. This approach offers an opportunity for early detection of transmission surges, allowing preparedness and potentially mitigating significant outbreaks at both spatial and temporal scales.

Keywords: Applied microbiology; Environmental monitoring; Molecular microbiology; Virology.

PubMed Disclaimer

Conflict of interest statement

No author declares any potential conflict of interest or competing financial or non-financial interest in relation to the manuscript.

Figures

**Figure 1**
Estimation of infection incidence and effective reproductive number for SARS-CoV-2 (A–D) (A) confirmed positive cases, (B) RNA concentration in wastewater, (C) comparison of daily SARS-CoV-2 confirmed cases, infection incidence estimated based on confirmed cases, and infection incidence estimated based on SARS-CoV-2 RNA concentration in wastewater for Bangkok, and (D) comparison of the effective reproductive numbers estimated using the case-based infection incidence (red line) and wastewater-based infection incidence (green line). The ribbons display the standard deviation of 1,000 bootstrap replicates.

**Figure 2**
Map for SARS-CoV-2 RNA in wastewater and reported cases (A–C) (A) confirmed positive SARS-CoV-2 cases, (B) SARS-CoV-2 RNA concentration in wastewater, and (C) percent of variant per total SARS-CoV-2 RNA concentration in wastewater.

**Figure 3**
Relative abundance of different SARS-CoV-2 viral variants in Wastewater SARS-CoV-2RNA concentration for each variant in wastewater and infection incidence estimated from each variant’s viral loads in wastewater for (A and B) Bangkok, (C and D) Nakhon Pathom, and (E and F) Rural areas. The ribbons show the standard deviation across 1,000 bootstrap replicates. (G) Relative abundance shows the transition of variants of viral loads in wastewater for each area.

**Figure 4**
SARS-CoV-2 RNA concentration in wastewater collected from different facilities (A–F) (A) Bangkok and (D) Rural areas. Relative abundance in SARS-CoV-2 RNA concentration in wastewater collected from different facilities in (C) Bangkok and (F) Rural areas. Infection incidences based on SARS-CoV-2 RNA concentration in (B) Bangkok and (E) Rural areas. The ribbons show the standard deviation of 1,000 bootstrap replicates. Gray areas show the period during a nationwide ban on large events to ease lockdown (26-Dec-20 to 29-Jan-21, and 17-Apr-21 to 01-Sep-21). The black labels show the superspreading events, and the red labels are the starting of interventions.

**Figure 5**
Relationship between SARS-CoV-2 RNA concentration in wastewater and reported cases (A) GCV values of the fitting models, the number of cases obtained from the best model (red line) compared to the reported cases (black dots) with their confidence intervals (ribbons) in (B) Total, (C) Bangkok, (D) Nakhon Pathom, (E) Nonthaburi, (F) Pathum Thani, (G) Samut Prakan, and (H) Samut Sakhon.

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[1] Pinilla J., Barber P., Vallejo-Torres L., Rodríguez-Mireles S., López-Valcárcel B.G., Serra-Majem L. The economic impact of the SARS-COV-2 (COVID-19) pandemic in Spain. Int. J. Environ. Res. Public Health. 2021;18:4708. doi: 10.3390/ijerph18094708. - DOI - PMC - PubMed

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[4] Liu F., Zhao Z., Ma C., Nie X., Wu A., Li X. Return to normal pre-COVID-19 life is delayed by inequitable vaccine allocation and SARS-CoV-2 variants. Epidemiol. Infect. 2022;150:e46. doi: 10.1017/s0950268822000139. - DOI - PMC - PubMed

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[7] Mills E.J., Reis G. Evaluating COVID-19 vaccines in the real world. Lancet. 2022;399:1205–1206. doi: 10.1016/S0140-6736(22)00194-5. - DOI - PMC - PubMed

[8] Mills E.J., Reis G. Evaluating COVID-19 vaccines in the real world. Lancet. 2022;399:1205–1206. doi: 10.1016/S0140-6736(22)00194-5. - DOI - PMC - PubMed

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[10] University J.H. Johns Hopkins University Coronavirus Resource Center; 2023. COVID 19 Dashboard.

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COVID-19 monitoring with sparse sampling of sewered and non-sewered wastewater in urban and rural communities

Affiliations

COVID-19 monitoring with sparse sampling of sewered and non-sewered wastewater in urban and rural communities

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Abstract

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