Journal of Korean Society on Water Environment (한국물환경학회지)

Korean Society on Water Environment (한국물환경학회)
권호 표지
DOI QR코드

DOI QR Code

Alternative and Rapid Detection Methods for Wastewater Surveillance of SARS-CoV-2

SARS-CoV-2의 하수조사를 위한 대체 및 신속 검출 방법

  • Jesmin Akter (Department of Environment Research, Korea Institute of Civil Engineering and Building Technology) ;
  • Bokjin Lee (Department of Environment Research, Korea Institute of Civil Engineering and Building Technology) ;
  • Jai-Yeop Lee (Department of Environment Research, Korea Institute of Civil Engineering and Building Technology) ;
  • Chang Hyuk Ahn (Department of Environment Research, Korea Institute of Civil Engineering and Building Technology) ;
  • Nishimura Fumitake (Research Center for Environmental Quality Management, Graduate School of Engineering, Kyoto University) ;
  • ILHO KIM (Department of Environment Research, Korea Institute of Civil Engineering and Building Technology)
  • 제스민아터 (한국건설기술연구원 환경연구본부) ;
  • 이복진 (한국건설기술연구원 환경연구본부) ;
  • 이재엽 (한국건설기술연구원 환경연구본부) ;
  • 안창혁 (한국건설기술연구원 환경연구본부) ;
  • ;
  • 김일호 (한국건설기술연구원 환경연구본부)
  • Received : 2023.09.08
  • Accepted : 2023.12.27
  • Published : 2024.01.30
Download PDF
⟨ Previous Next ⟩

Abstract

The global pandemic, coronavirus disease caused by Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has led to the implementation of wastewater surveillance as a means to monitor the spread of SARS-CoV-2 prevalence in the community. The challenging aspect of establishing wastewater surveillance requires a well-equipped laboratory for wastewater sample analysis. According to previous studies, RT-PCR-based molecular tests are the most widely used and popular detection method worldwide. However, this approach for the detection or quantification of SARS-CoV-2 from wastewater demands a specialized laboratory, skilled personnel, expensive instruments, and a workflow that typically takes 6 to 8 hours to provide results for a few samples. Rapid and reliable alternative detection methods are needed to enable less-well-qualified practitioners to set up and provide sensitive detection of SARS-CoV-2 within wastewater at regional laboratories. In some cases, the structural and molecular characteristics of SARS-CoV-2 are unknown, and various strategies for the correct diagnosis of COVID-19 have been proposed by research laboratories. The ongoing research and development of alternative and rapid technologies, namely RT-LAMP, ELISA, Biosensors, and GeneXpert, offer a wide range of potential options not only for SARS-CoV-2 detection but also for other viruses. This study aims to discuss the effective regional rapid detection and quantification methods in community wastewater.

Keywords

Acknowledgement

This research was supported by National R&D Program through the National Research Foundation of Korea(NRF) funded by Ministry of Science and ICT(NRF-2021K1A4A8A 01079319)

References

  1. Adriaenssens, E. M., Farkas, K., Harrison, C., Jones, D. L., Allison, H. E., and McCarthy, A. J. (2018). Viromic analysis of wastewater input to a river catchment reveals a diverse assemblage of RNA viruses, mSystems, 3(3), e00025-18.
  2. Ahmed, W., Angel, N., Edson, J., Bibby, K., Bivins, A., O'Brien, J. W., Choi, P. M., Kitajima, M., Simpson, S. L., Li, J., Tscharke, B., Verhagen, R., Smith, W. J. M., Zaugg, J., Dierens, L., Hugenholtz, P., Thomas, K. V., and Mueller, J. F. (2020). First confirmed detection of SARSCoV-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, 138764.
  3. Ahmed, W., Bertsch, P. M., Bivins, A., Bibby, K., Farkas, K., Gathercole, A., Haramoto, E., Gyawali, P., Korajkic, A., McMinn, B. R., Mueller, J. F., Simpson, S. L., Smith, W. J. M., Symonds, E. M., Thomas, K. V., Verhagen, R., and Kitajima, M. (2020). Comparison of virus concentration methods for the RT-qPCR-based recovery of murine hepatitis virus, a surrogate for SARS-CoV-2 from untreated wastewater, Science of the Total Environment, 739, 139960.
  4. Ahmed, W., Bivins, A., Bertsch, P. M., Bibby, K., Choi, P. M., Farkas, K., Gyawali, P., Hamilton, K. A., Haramoto, E., Kitajima, M., Simpson, S. L., Tandukar, S., Thomas, K., and Mueller, J. F. (2020). Surveillance of SARS-CoV-2 RNA in wastewater: Methods optimisation and quality control are crucial for generating reliable public health information, Current Opinion in Environmental Science & Health, 17, 82-93. https://doi.org/10.1016/j.coesh.2020.09.003
  5. Ahmed, W., Simpson, S. L., Bertsch, P. M., Bibby, K., Bivins, A., Blackall, L. L., Bofill-Mas, S., Bosch, A., Brandao, J., Choi, P. M., Ciesielski, M., Donner, E., D'Souza, N., Farnleitner, A. H., Gerrity, D., Gonzalez, R., Griffith, J. F., Gyawali, P., Haas, C. N., Hamilton, K. A., ... and Shanks, O. C. (2022). Minimizing errors in RT-PCR detection and quantification of SARS-CoV-2 RNA for wastewater surveillance, Science of the Total Environment, 805, 149877.
  6. Ahmed, W., Smith, W. J. M., Metcalfe, S., Jackson, G., Choi, P. M., Morrison, M., Field, D., Gyawali, P., Bivins, A., Bibby, K., and Simpson, S. L. (2022). Comparison of RT-qPCR and RT-dPCR Platforms for the trace detection of SARS-CoV-2 RNA in wastewater, ACS ES&T Water, 2(11), 1871-1880.
  7. Ahn, S. J., Baek, Y. H., Lloren, K. K. S., Choi, W. S., Jeong, J. H., Antigua, K. J. C., Kwon, H. I., Park, S. J., Kim, E. H., Kim, Y. I., Si, Y. J., Hong, S. B., Shin, K. S., Chun, S., Choi, Y. K., and Song, M. S. (2019). Rapid and simple colorimetric detection of multiple influenza viruses infecting humans using a reverse transcriptional loop-mediated isothermal amplification (RT-LAMP) diagnostic platform, BMC Infectious Diseases, 19(1), 676.
  8. Alexander, M. R., Rootes, C. L., van Vuren, P. J., and Stewart, C. R. (2020). Concentration of infectious SARS-CoV-2 by polyethylene glycol precipitation, Journal of Virological Methods, 286, 113977.
  9. Amaral, C., Antunes, W., Moe, E., Duarte, A. G., Lima, L. M. P., Santos, C., Gomes, I. L., Afonso G. S., Vieira, R., Teles, H. S. S., Reis, M. S., Ramalho da Silva, M. A., Henriques, A. M., Fevereiro, M.,Ventura, M. R., Serrano, M., and Pimentel, C. (2021). A molecular test based on RT LAMP for rapid, sensitive and inexpensive colorimetric detection of SARS-CoV-2 in clinical samples, Scientific Reports, 11(1), 16430.
  10. Amdiouni, H., Maunula, L., Hajjami, K., Faouzi, A., Soukri, A., and Nourlil, J. (2012). Recovery comparison of two virus concentration methods from wastewater using cell culture and real-time PCR, Current Microbiology, 65(40), 432-437. https://doi.org/10.1007/s00284-012-0174-8
  11. Amoah, D., I., Mthethwa, P., N., Pillay, L., Deepnarain, N., Pillay, K., Awolusi, O., O., Kumari, S., and Bux, F. (2021). RT LAMP: A cheaper, simpler and faster alternative for the detection of SARS-CoV-2 in wastewater, Food and Environmental Virology, 13(4), 447-456. https://doi.org/10.1007/s12560-021-09489-7
  12. Anahtar, M. N., McGrath, G. E. G., Rabe, B. A., Tanner, N. A., White, B. A., Lennerz, J. K. M., Branda, J. A., Cepko, C. L., and Rosenberg, E. S. (2020). Clinical assessment and validation of a rapid and sensitive SARS-CoV-2 test using reverse-transcription loop-mediated isothermal amplification without the need for RNA Extraction, Open Forum Infectious Diseases, 8(2), ofaa631.
  13. Ando, H., Iwamoto, R., Kobayashi, H., Okabe, S., and Kitajima, M. (2022). The efficient and practical virus identification system with enhanced sensitivity for solids (EPISENS-S): A rapid and cost-effective SARS-CoV-2 RNA detection method for routine wastewater surveillance, Science of The Total Environment, 843, 157101.
  14. Artika, I. M., Wiyatno, A., and Ma'roef, C. N. (2020). Pathogenic viruses: Molecular detection and characterization, Infection, Genetics and Evolution, 81, 104215.
  15. Asghar, H., Diop, O. M., Weldegebriel, G., Malik, F., Shetty, S., El Bassioni, L., Akande, A. O., Al Maamoun, E., Zaidi, S., Adeniji, A. J., Burns, C. C., Deshpande, J., Oberste, M. S., and Lowther, S. A. (2014). Environmental surveillance for polioviruses in the global polio eradication initiative, The Journal of Infectious Diseases, 210, S294-S303. https://doi.org/10.1093/infdis/jiu384
  16. Assis, A. S. F., Fumian, T. M., Miagostovich, M. P., Drumond, B. P., and da Rosa E Silva, M. L. (2018). Adenovirus and rotavirus recovery from a treated effluent through an optimized skimmed-milk flocculation method, Environmental Science and Pollution Research International, 25(17), 17025-17032. https://doi.org/10.1007/s11356-018-1873-x
  17. Atha, D. H. and Ingham, K. C. (1981). Mechanism of precipitation of proteins by polyethylene glycols. analysis in terms of excluded volume, Journal of Biological Chemistry, 256, 12108-12117. https://doi.org/10.1016/S0021-9258(18)43240-1
  18. Barbosa, C., Nogueira, S., Gadanho, M., and Chaves, S. (2016). Chapter7-DNA extraction: finding the most suitable method, Molecular Microbial Diagnostic Methods, Elsevier, 135-154.
  19. Bar-Or, I., Yaniv, K., Shagan, M., Ozer, E., Erster, O., Mendelson, E., Mannasse, B., Shirazi, R., Kramarsky-Winter, E., Nir, O., Abu-Ali, H., Ronen, Z., Rinott, E., Lewis, Y., Friedler, E. F., Paitan, Y., Bitkover, E., Berchenko, Y., and Kushmaro, A. (2020). Regressing SARSCoV-2 sewage measurements onto COVID-19 burden in the population: A proof-of-concept for quantitative environmental surveillance, medRxiv, 2020.04.26.20073569.
  20. Barril, P. A., Pianciola, L. A., Mazzeo, M., Ousset, M. J., Jaureguiberry, M. V., Alessandrello, M., Sanchez, G., and Oteiza, J. M. (2021). Evaluation of viral concentration methods for SARS- CoV-2 recovery from wastewaters, Science of the Total Environment, 756, 144105.
  21. Beattie, R. E., Blackwood, A. D., Clerkin, T., Dinga, C., and Noble, R., T. (2022). Evaluating the impact of sample storage, handling, and technical ability on the decay and recovery of SARS-CoV-2 in wastewater, PLoS ONE, 17(6), e0270659.
  22. Becker, M. G., Taylor, T., Kiazyk, S., Cabiles, D. R., Meyers, A. F. A., and Sandstrom, P. A. (2020). Recommendations for sample pooling on the Cepheid GeneXpert® system using the Cepheid Xpert® Xpress SARS-CoV-2 assay, PLoS ONE, 15(11), e0241959.
  23. Bertrand, I., Challant, J., Jeulin, H., Hartard, C., Mathieu, L., Lopez, S., Scientific Interest Group Obepine, Schvoerer, E., Courtois, S., and Gantzer, C. (2021). Epidemiological surveillance of SARS-CoV-2 by genome quantification in wastewater applied to a city in the northeast of France: Comparison of ultrafiltration-and protein precipitation-based methods, International Journal of Hygiene and Environmental Health, 233, 113692.
  24. Bhadra, S., Jiang, Y. S., Kumar, M. R., Johnson, R. F., Hensley L. E., and Ellington, A. D. (2015). Real-time sequence-validated loop-mediated isothermal amplification assays for detection of Middle East respiratory syndrome coronavirus (MERS-CoV), PLoS ONE, 10, e0123126.
  25. Boonham, N., Kreuze, J., Winter, S., van der Vlugt, R., Bergervoet, J., Tomlinson, J., and Mumford, R. (2014). Methods in virus diagnostics: from ELISA to next generation sequencing, Virus Research, 186, 20-31. https://doi.org/10.1016/j.virusres.2013.12.007
  26. Buck, M. D., Poirier, E. Z., Cardoso, A., Frederico, B., Canton, J., Barrell, S., Beale, R. C., Byrne, R., Caidan, S., Crawford, M., Cubitt, L., Gandhi, S., Goldstone, R. L., Grant, P. R., Gulati, K., Hindmarsh, S., Howell, M., Hubank, M., Instrell, R., Jiang, M., Kassiotis, G., Lu, W., MacRae, J. I., Martini, I., Miller, D., Moore, D., Nastouli, E., Nicod, J., Nightingale, L., Olsen, J., Oomatia, A., O'Reilly, N. J., Rideg, A., Song, O., Strange, A., Swanton, C., Turajlic, S., Wu, M.Y., and Reis e Sousa, C. (2020). Standard operating procedures for SARS-CoV-2 detection by a clinical diagnostic RT-LAMP assay, medRxiv, 2020.06.29.20142430.
  27. Butler, D. J., Mozsary, C., Meydan, C., Danko, D., Foox, J., Rosiene, J., Shaiber, A., Afshinnekoo, E., MacKay, M., Sedlazeck, F. J., Ivanov, N. A., Sierra, M., Pohle, D., Zietz, M., Gisladottir, U., Ramlall, V., Westover, C. D., Ryon, K., Young, B., Bhattacharya, C., ... and Mason, C. E. (2020). Shotgun transcriptome and isothermal profiling of SARS-CoV-2 infection reveals unique host responses, viral diversification, and drug interactions, bioRxiv, 2020.04.20.048066.
  28. Butler, J. M. (2010). Chapter 5-DNA extraction, fundamentals of forensic typing, Elsevier, 99-109.
  29. Calgua, B., Mengewein, A., Grunert, A., Bofill-Mas, S., Clemente-Casares, P., Hundesa, A., Wyn-Jones, A. P., Lopez-Pila, J. M., and Girnones, R. (2008). Development and application of a one-step low-cost procedure to concentrate viruses from seawater samples, Journal of Virological Methods, 153(2), 79-83. https://doi.org/10.1016/j.jviromet.2008.08.003
  30. Calgua, B., Rodriguez-Manzano, J., Hundesa, A., Sunen, E., Calvo, M., Bofill-Mas, S., and Girones, R. (2013). New methods for the concentration of viruses from urban sewage using quantitative PCR, Journal of Virological Methods, 187(2), 215-221. https://doi.org/10.1016/j.jviromet.2012.10.012
  31. Cao, Y., Griffith, J. F., Dorevitch, S., and Weisberg, S. B. (2012). Effectiveness of qPCR permutations, internal controls and dilution as means for minimizing the impact of inhibition while measuring Enterococcus in environmental waters, Journal of Applied Microbiology, 113(1), 66-75. https://doi.org/10.1111/j.1365-2672.2012.05305.x
  32. Carrillo-Reyes, J., Barragan-Trinidad, M., and Buitron, G. (2021). Surveillance of SARS-CoV-2 in sewage and wastewater treatment plants in Mexico, Journal of Water Process Engineering, 40, 101815.
  33. Chavarria-Miro, G., Anfruns-Estrada, E., Martinez-Velazquez, A., Vazquez-Portero, M., Guix, S., Paraira, M., Galofre, B., Sanchez, G., Pinto, R. M., and Bosch, A. (2021). Time-evolution of SARS-CoV-2 in wastewater during the first pandemic wave of COVID- 19 in the metropolitan area of Barcelona, Applied and Environmental Microbiology, 87(7), e02750-20.
  34. Ciesielski, M., Blackwood, D., Clerkin, T., Gonzalez, R., Thompson, H., Larson, A., and Noble, R. (2021). Assessing sensitivity and reproducibility of RT-dd PCR and RT-qPCR for the quantification of SARS-CoV-2 in wastewater, Journal of Virological Methods, 297, 114230.
  35. Cox, K. L., Devanarayan, V., Kriauciunas, A., Manetta, J., Montrose, C., and Sittampalam, S. (2012). Immunoassay Methods, Eli Lilly & Company and the National Center for Advancing Translational Sciences, Bethesda (MD).
  36. D'Aoust, P. M., Mercier, E., Montpetit, D., Jia, J. J., Alexandrov, I., Neault, N., Baig, A. T., Mayne, J., Zhang, X., Alain, T., Langlois, M. A., Servos, M. R., MacKenzie, M., Figeys, D., MacKenzie, A. E., Graber, T. E., and Delatolla, R. (2021). Quantitative analysis of SARS-CoV-2 RNA from wastewater solids in communities with low COVID-19 incidence and prevalence, Water Research, 188, 116560.
  37. Daigle, J., Racher, K., Hazenberg, J., Yeoman, A., Hannah, H., Duong, D., Mohammed, U., Spreitzer, D., Gregorchuk, B. S. J., Head, B. M., Meyers, A. F. A., Sandstrom, P. A., Nichani, A., Brooks, J. I., Mulvey, M. R., Mangat, C. S., and Becker, M. G. (2022). A sensitive and rapid wastewater test for SARS-COV-2 and its use for the early detection of a cluster of cases in a remote community, Applied and environmental microbiology, 88(5), e0174021.
  38. Dao Thi, V. L., Herbst, K., Boerner, K., Meurer, M., Kremer, L. P., Kirrmaier, D., Freistaedter, A., Papagiannidis, D., Galmozzi, C., Stanifer, M. L., Boulant, S., Klein, S., Chlanda, P., Khalid, D., Barreto Miranda, I., Schnitzler, P., Krausslich, H. G., Knop, M., and Anders, S. (2020). A colorimetric RT-LAMP assay and LAMP-sequencing for detecting SARS-CoV-2 RNA in clinical samples, Science Translational Medicine, 12(556), eabc7075.
  39. Dhama, K., Karthik, K., Chakraborty, S., Tiwari, R., Kapoor, S., Kumar, A., and Thomas, P. (2014). Loop mediated isothermal amplification of DNA (LAMP): A new diagnostic tool lights the world of diagnosis of animal and human pathogens: A review, Pakistan Journal of Biological Sciences: PJBS, 17(2), 151-166. https://doi.org/10.3923/pjbs.2014.151.166
  40. Di Bonito, P., Iaconelli, M., Gheit, T., Tommasino, M., Della Libera, S., Bonadonna, L., and La Rosa, G. (2017). Detection of oncogenic viruses in water environments by a Luminex-based multiplex platform for high throughput screening of infectious agents, Water Research, 123, 549-555. https://doi.org/10.1016/j.watres.2017.06.088
  41. Dundas, N., Leos, N. K., Mitui, M., Revell, P., and Rogers, B. B. (2008). Comparison of automated nucleic acid extraction methods with manual extraction, The Journal of Molecular Diagnostics: JMD, 10(4), 311-316. https://doi.org/10.2353/jmoldx.2008.070149
  42. Fernandez-de-Mera, I. G., Rodriguez Del-Rio, F. J., de la Fuente, J., Perez-Sancho, M., Hervas, D., Moreno, I., Dominguez, M., Dominguez, L., and Gortazar, C. (2021). Detection of environmental SARS-CoV-2 RNA in a high prevalence setting in Spain, Transboundary and Emerging Diseases, 68(3), 1487-1492. https://doi.org/10.1111/tbed.13817
  43. Fischbach, J., Xander, N. C., Frohme, M., and Glokler, J. F. (2015). Shining a light on LAMP assays - A comparison of LAMP visualization methods including the novel use of berberine, BioTechniques, 58(4), 189-194. https://doi.org/10.2144/000114275
  44. Gan, S. D. and Patel, K. R. (2013). Enzyme immunoassay and enzyme-linked immunosorbent assay, The Journal of investigative dermatology, 133(9), e12.
  45. Gerrity, D., Papp, K., Stoker, M., Sims, A., and Frehner, W. (2021). Early pandemic wastewater surveillance of SARS-CoV-2 in southern Nevada: Methodology, occurrence, and incidence/prevalence considerations, Water research X, 10, 100086.
  46. Gibas, C., Lambirth, K., Mittal, N., Juel, M. A. I., Barua, V. B., Roppolo Brazell, L., Hinton, K., Lontai, J., Stark, N., Young, I., Quach, C., Russ, M., Kauer, J., Nicolosi, B., Chen, D., Akella, S., Tang, W., Schlueter, J., and Munir, M. (2021). Implementing building-level SARS-CoV-2 wastewater surveillance on a university campus, Science of the Total Environment, 782, 146749.
  47. Goto, M., Honda, E., Ogura, A., Nomoto, A. and Hanaki, K. (2009). Colorimetric detection of loop-mediated isothermal amplification reaction by using hydroxy naphthol blue, Biotechniques, 46, 167-172. https://doi.org/10.2144/000113072
  48. Graham, K. E., Loeb, S. K., Wolfe, M. K., Catoe, D., Sinnott-Armstrong, N., Kim, S., Yamahara, K. M., Sassoubre, L. M., Mendoza Grijalva, L. M., Roldan-Hernandez, L., Langenfeld, K., Wigginton, K. R., and Boehm, A. B. (2021). SARS-CoV-2 RNA in wastewater dettled dolids is associated with COVID-19 cases in a large urban sewershed, Environmental Science & Technology, 55(1), 488-498. https://doi.org/10.1021/acs.est.0c06191
  49. Guttman, B. (2013). Virus. Brenner's Encyclopedia of Genetics, Elsevier, 291-294.
  50. Haramoto, E., Kitajima, M., Hata, A., Torrey, J. R., Masago, Y., Sano, D., and Katayama, H. (2018). A review on recent progress in the detection methods and prevalence of human enteric viruses in water, Water Research, 135, 168-186. https://doi.org/10.1016/j.watres.2018.02.004
  51. 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, The Science of the Total environmental biology, 737, 140405.
  52. Hata, A., Hara-Yamamura, H., Meuchi, Y., Imai, S., and Honda, R. (2021). Detection of SARS-CoV-2 in wastewater in Japan during a COVID-19 outbreak, The Science of the Total Environment, 758, 143578.
  53. Hellmer, M., Paxeus, N., Magnius, L., Enache, L., Arnholm, B., Johansson, A., Bergstrom, T., and Norder, H. (2014). Detection of pathogenic viruses in sewage provided early warnings of hepatitis A virus and norovirus outbreaks, Applied and Environmental Microbiology, 80(21), 6771-6781. https://doi.org/10.1128/AEM.01981-14
  54. Hong, T. C., Mai, Q. L., Cuong, D. V., Parida, M., Minekawa, H., Notomi, T., Hasebe, F., and Morita, K. (2004). Development and evaluation of a novel loop-mediated isothermal amplification method for rapid detection of severe acute respiratory syndrome coronavirus, Journal of Clinical Microbiology, 42(5), 1956-1961. https://doi.org/10.1128/JCM.42.5.1956-1961.2004
  55. Hsieh, K., Mage, P. L., Csordas, A. T., Eisenstein, M., and Soh, H. T. (2014). Simultaneous elimination of carryover contamination and detection of DNA with uracil-DNA-glycosylase-supplemented loop-mediated isothermal amplification (UDG-LAMP), Chemical Communications, 50, 3747-3749. https://doi.org/10.1039/c4cc00540f
  56. Huang, W. E., Lim, B., Hsu, C. C., Xiong, D., Wu, W., Yu, Y., Jia, H., Wang, Y., Zeng, Y., Ji, M., Chang, H., Zhang, X., Wang, H., and Cui, Z. (2020). RT-LAMP for rapid diagnosis of coronavirus SARS-CoV-2, Microbial Biotechnology, 13(4), 950-961. https://doi.org/10.1111/1751-7915.13586
  57. Ibrahim, C., Hammami, S., Mejri, S., Mehri, I., Pothier, P., and Hassen, A. (2017). Detection of Aichi virus genotype B in two lines of wastewater treatment processes, Microbial Pathogenesis, 109, 305-312. https://doi.org/10.1016/j.micpath.2017.06.001
  58. Ibrahim, N., Jamaluddin, N. D., Tan, L. L., and Mohd Yusof, N. Y. (2021). A review on the development of gold and silver nanoparticles-dased biosensor as a detection strategy of emerging and pathogenic RNA virus, Sensors (Basel, Switzerland), 21(15), 5114.
  59. Islam, G., Gedge, A., Lara-Jacobo, L., Kirkwood, A., Simmons, D., and Desaulniers, J. P. (2022). Pasteurization, storage conditions and viral concentration methods influence RT-qPCR detection of SARS-CoV-2 RNA in wastewater, Science of the Total Environment, 821, 153228.
  60. Jayawardena, S., Cheung, C. Y., Barr, I., Chan, K. H., Chen, H., Guan, Y., Peiris, J. S., and Poon, L. L. (2007). Loop-mediated isothermal amplification for influenza A (H5N1) virus, Emerging Infectious Diseases, 13(6), 899-901. https://doi.org/10.3201/eid1306.061572
  61. Johnson, G., Zubrzycki, A., Henry, M., Ranadheera, C., Corbett, C., Meyers, A. F. A., Sandstrom, P. A., and Becker, M. G. (2021). Clinical evaluation of the GeneXpert® Xpert® Xpress SARS-CoV-2/Flu/RSV combination test, Journal of Clinical Virology Plus, 1(1), 100014.
  62. Katsarou, K., Bardani, E., Kallemi, P., and Kalantidis, K. (2019). Viral detection: Past, present, and future, BioEssays, 41(10), e1900049.
  63. Kellner, M. J., Ross, J. J., Schnabl, J., Dekens, M. P. S., Matl, M., Heinen, R., Grishkovskaya, I., Bauer, B., Stadlmann, J., Menendez-Arias, L., Straw, A. D., Fritsche-Polanz, R., Traugott, M., Seitz, T., Zoufaly, A., Fodinger, M., Wenisch, C., Zuber, J., Pauli, A., and Brennecke, J. (2020). A rapid, highly sensitive and open-access SARS-CoV-2 detection assay for laboratory and home testing, Frontiers in Molecular Biosciences, 9, 801309.
  64. Kim, S., Kennedy, L. C., Wolfe, M. K., Criddle, C. S., Duong, D. H., Topol, A., White, B. J., Kantor, R. S., Nelson, K. L., Steele, J. A., Langlois, K., Griffith, J. F., Zimmer-Faust, A. G., McLellan, S. L., Schussman, M. K., Ammerman, M., Wigginton, K. R., Bakker, K. M., and Boehm, A. B. (2022). SARS-CoV-2 RNA is enriched by orders of magnitude in primary settled solids relative to liquid wastewater at publicly owned treatment works, Environmental Science: Water Research & Technology, 8, 757-770. https://doi.org/10.1039/D1EW00826A
  65. Kitajima, M., Sassi, H. P., and Torrey, J. (2018). Pepper mild mottle virus as a water quality indicator, npj Clean Water, 1, 1-9. https://doi.org/10.1038/s41545-018-0001-2
  66. Kocamemi, B. A., Kurt, H., Hacioglu, S., Yarali, C., Saatci, A. M., and Pakdemirli, B. (2020). First dataset on SARS-CoV-2 detection for Istanbul wastewaters in Turkey, medRxiv, 2020.05.03.20089417.
  67. Kojabad, A. A., Farzanehpour, M., Galeh, H. E. G., Dorostkar, R., Jafarpour, A., Bolandian, M., and Nodooshan, M. M. (2021). Droplet digital PCR of viral DNA/RNA, current progress, challenges, and future perspectives, Journal of Medical Virology, 93(7), 4182-4197. https://doi.org/10.1002/jmv.26846
  68. Kumar, M., Patel, A. K., Shah, A. V., Raval, J., Rajpara, N., Joshi, M., and Joshi, C. J. (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, 141326.
  69. Kumar, R., Singh, R., Hui, D., Feo, L., and Fraternali, F. (2018). Graphene as biomedical sensing element: State of art review and potential engineering applications, Composites Part B: Engineering, 134, 193-206. https://doi.org/10.1016/j.compositesb.2017.09.049
  70. La Rosa, G., Iaconelli, M., Mancini, P., Bonanno Ferraro, G., Veneri, C., Bonadonna, L., Lucentini, L., and Suffredini, E. (2020). First detection of SARS-CoV-2 in untreated wastewaters in Italy, Science of the Total Environment, 736, 139652.
  71. Lamb, L. E., Bartolone, S. N., Ward, E., and Chancellor, M. B., (2020). Rapid detection of novel coronavirus/Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) by reverse transcription-loop-mediated isothermal amplification, PLoS One, 15(6), e0234682.
  72. Larsen, D. A. and Wigginton, K. R. (2020). Tracking COVID-19 with wastewater, Nature Biotechnology, 38(10), 1151-1153. https://doi.org/10.1038/s41587-020-0690-1
  73. LaTurner, Z. W., Zong, D. M., Kalvapalle, P., Gamas, K. R., Terwilliger, A., Crosby, T., Ali, P., Avadhanula, V., Santos, H. H., Weesner, K., Hopkins, L., Piedra, P. A., Maresso, A. W., and Stadler, L. B. (2021). Evaluating recovery, cost, and throughput of different concentration methods for SARS-CoV-2 wastewater-based epidemiology, Water Research, 197, 117043.
  74. Lee, S. H., Baek, Y. H., Kim, Y. H., Choi, Y. K., Song, M. S., and Ahn, J. Y. (2017). One-pot reverse transcriptional loop-mediated isothermal amplification (RT-LAMP) for detecting MERS-CoV, Frontiers in microbiology, 7, 2166.
  75. Lewis, G. D. and Metcalf, T. G. (1988). Polyethylene glycol precipitation for recovery of pathogenic viruses, including hepatitis a virus and human rotavirus, from oyster, water, and sediment samples, Applied and Environmental Microbiology, 54(8), 1983-1988. https://doi.org/10.1128/aem.54.8.1983-1988.1988
  76. Lino, A., Cardoso, M. A., Goncalves, H. M. R., and Martins-Lopes, P. (2022). SARS-CoV-2 detection methods, Chemosensors, 10(6), 221.
  77. Lv, H., Wu, N. C., Tsang, O. T. Y., Yuan, M., Perera, R. A. P. M., Leung, W. S., So, R. T. Y., Chan, J. M. C., Yip, G. K., Chik, T. S. H., Wang, Y., Choi, C. Y. C., Lin, Y., Ng, W. W., Zhao, J., Poon, L. L. M., Peiris, M., Wilson, I. A., and Mok, C. K. P. (2020). Cross-reactive antibody response between SARS-CoV-2 and SARS-CoV infections, Cell Reports, 31, 107725.
  78. Masclaux, F. G., Hotz, P., Friedli, D., Savova-Bianchi, D., and Oppliger, A. (2013). High occurrence of hepatitis E virus in samples from wastewater treatment plants in Switzerland and comparison with other enteric viruses, Water Research, 47(14), 5101-5109. https://doi.org/10.1016/j.watres.2013.05.050
  79. 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(7), 511-516. https://doi.org/10.1021/acs.estlett.0c00357
  80. Misra, R., Acharya, S., and Sushmitha, N. (2021). Nano biosensor-based diagnostic tools in viral infections: Special emphasis on COVID-19, Reviews in Medical Virology, 32(2), e2267.
  81. Murphy, F. A. (1988). Virus raxonomy and nomenclature. In: laboratory diagnosis of infectious diseases principles and practice, Springer, New York, NY, 153-176.
  82. Nagamine, K., Hase, T., and Notomi, T. (2002). Accelerated reaction by loop-mediated isothermal amplification using loop primers, Molecular and Cellular Probes, 16(3), 223-229. https://doi.org/10.1006/mcpr.2002.0415
  83. Naughton, C. C., Roman, F. A., Alvarado, A. G. F., Tariqi, A. Q., Deeming, M. Q., Bibby, K. Bivins, A. Rose, J. B., Medema, G. Ahmed, W., Katsivelis, P., Allan, V., Sinclair, R., Zhang, Y., and Kinyua, M. N. (2021). Show us the data: Global COVID-19 wastewater monitoring efforts, equity, and gaps, MedRxiv.
  84. Navarro, A., Gomez, L., Sanseverino, I., Niegowska, M., Roka, E., Pedraccini, R., Vargha, M., and Lettieri, T. (2021). SARS-CoV-2 detection in wastewater using multiplex quantitative PCR, Science of the Total Environment, 797, 148890.
  85. Ng, T.F.F., Marine, R., Wang, C., Simmonds, P., Kapusinszky, B., Bodhidatta, L., Oderinde, B. S., Wommack, K. E., and Delwart, E. (2012). High variety of known and new RNA and DNA viruses of diverse origins in untreated sewage, Journal of Virology, 86(22), 12161-12175. https://doi.org/10.1128/JVI.00869-12
  86. Notomi, T., Mori, Y. H., Tomita, N., and Kanda, H. (2015). Loop-mediated isothermal amplification (LAMP): Principle, features, and future prospects, Journal of Microbiology, 53(1), 1-5. https://doi.org/10.1007/s12275-015-4656-9
  87. Notomi, T., Okayama, H., Masubuchi, H., Yonekawa, T., Watanabe, K., Amino, N., and Hase, T. (2000). Loop-mediated isothermal amplification of DNA, Nucleic Acids Research, 28(12), E63.
  88. O'Carroll, I. P. and Rein, A. (2016). Viral nucleic acids, Encyclopedia of Cell Biology, 517-524.
  89. Park, G. S., Ku, K., Baek, S. H., Kim, S. J., Kim, S. I., Kim, B. T., and Maeng, J. S. (2020). Development of reverse transcription loop-mediated isothermal amplification assays targeting severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), The Journal of Molecular Diagnostics, 22(6),729-735. https://doi.org/10.1016/j.jmoldx.2020.03.006
  90. Pecson, B. M., Darby, E., Haas, C. N., Amha, Y. M., Bartolo, M., Danielson, R., Dearborn, Y., Di Giovanni, G., Ferguson, C., Fevig, S., Gaddis, E., Gray, D., Lukasik, G., Mull, B., Olivas, L., Olivieri, A., Qu, Y., and SARS-CoV-2 Interlaboratory Consortium. (2021). Reproducibility and sensitivity of 36 methods to quantify the SARS-CoV-2 genetic signal in raw wastewater: Findings from an interlaboratory methods evaluation in the US, Environmental Science : Water Research & Technology, 7, 504-520. https://doi.org/10.1039/D0EW00946F
  91. Perez-Cataluna, A., Cuevas-Ferrando, E., Randazzo, W., Falco, I., Allende, A., and Sanchez, G. (2021). Comparing analytical methods to detect SARS-CoV-2 in wastewater, Science of the Total Environment, 758, 143870.
  92. Philo, S. E., Keim, E. K., Swanstrom, R., Ong, A. Q. W., Burnor, E. A., Kossik, A. L., Harrison, J. C., Demeke, B. A., Zhou, N. A., Beck, N. K., Shirai, J. H., and Meschke, J. S. (2021). A comparison of SARS-CoV-2 wastewater concentration methods for environmental surveillance, Science of the Total Environment, 760, 144215.
  93. Prado, T., Fumian, T. M., Mannarino, C. F., Maranhao, A. G., Siqueira, M. M., and Miagostovich, M. P. (2020). Preliminary results of SARS- CoV-2 detection in sewerage system in Niteroi municipality, Rio de Janeiro, Brazil, Memorias do Instituto Oswaldo Cruz, 115, e200196.
  94. Quyen, T. L., Ngo, T. A., Bang, D. D., Madsen, M., and Wolff, A. (2019). Classification of multiple DNA dyes based on inhibition effects on real-time loop-mediated isothermal amplification (LAMP): Prospect for point of care setting, Frontiers in Microbiology, 10, 2234.
  95. Rabe, B. A. and Cepko, C. (2020). SARS-CoV-2 detection using isothermal amplification and a rapid, inexpensive protocol for sample inactivation and purification, Proceedings of the National Academy of Sciences of the United States of America, 117(39),24450-24458. https://doi.org/10.1073/pnas.2011221117.
  96. Randazzo, W., Truchado, P., Cuevas-Ferrando, E., Simon, P., Allende, A., and Sanchez G. (2020). SARS-CoV-2 RNA in wastewater anticipated COVID-19 occurrence in a low prevalence area, Water Research, 181, 115942.
  97. Rimoldi, S. G., Stefani, F., Gigantiello, A., Polesello, S., Comandatore, F., Mileto, D., Maresca, M., Longobardi, C., Mancon, A., Romeri, F., Pagani, C., Cappelli, F., Roscioli, C., Moja, L., Gismondo, M. R., and Salerno, F. (2020). Presence and infectivity of SARS-CoV-2 virus in wastewaters and rivers, Science of the Total Environment, 744, 140911.
  98. Salvo, M., Moller, A., Alvareda, E., Gamazo, P., Colina, R., and Victoria, M. (2021). Evaluation of low-cost viral concentration methods in wastewaters: Implications for SARS-CoV-2 pandemic surveillances, Journal of Virological Methods, 297, 114249.
  99. Sapula, S. A., Whittall, J. J., Pandopulos, A. J., Gerber, C., and Venter, H. (2021). An optimized and robust PEG precipitation method for detection of SARS-CoV-2 in wastewater, Science of the Total Environment, 785, 147270.
  100. Schrader, C., Schielke, A., Ellerbroek, L., and Johne, R. (2012). PCR inhibitors - occurrence, properties, and removal, Journal of Applied Microbiology, 113(5), 1014-1026. https://doi.org/10.1111/j.1365-2672.2012.05384.x
  101. Sherchan, S. P., Shahin, S., Ward, L. M., Tandukar, S., Aw, T. G., Schmitz, B., Ahmed, W., and Kitajima, M. (2020). First detection of SARS-CoV-2 RNA in wastewater in North America: A study in Louisiana, USA, Science of the Total Environment, 743, 140621.
  102. Shieh, Y. S., Wait, D., Tai, L., and Sobsey, M. D. (1995). Methods to remove inhibitors in sewage and other fecal wastes for enterovirus detection by the polymerase chain reaction, Journal of Virological Methods, 54(1), 51-66. https://doi.org/10.1016/0166-0934(95)00025-P
  103. Tanner, N. A., Zhang, Y., and Evans, T. C. Jr. (2015). Visual detection of isothermal nucleic acid amplification using pH-sensitive dyes, Biotechniques, 58(2), 59-68. https://doi.org/10.2144/000114253
  104. Thompson, D. and Lei, Y. (2020). Recent progress in RT-LAMP enabled COVID-19 detection, Sensors and Actuators Reports, 2(1), 100017.
  105. Tiwari, A., Ahmed, W., Oikarinen, S., Sherchan, S., P., Heikinheimo, A., Jiang, G., Simpson S., L., Greaves, J., and Bivins, A. (2022). Application of digital PCR for public health-related water quality monitoring, Science of the Total Environment, 837, 155663.
  106. Tomita, N., Mori, Y., Kanda, H., and Notomi, T. (2008). Loop-mediated isothermal amplification (LAMP) of gene sequences and simple visual detection of products, Nature Protocols, 3(5), 877-882. https://doi.org/10.1038/nprot.2008.57
  107. Torii, S., Furumai, H., and Katayama, H. (2021). Applicability of polyethylene glycol precipitation followed by acid guanidinium thiocyanate-phenol-chloroform extraction for the detection of SARS-CoV-2 RNA from municipal wastewater, Science of the Total Environment, 756, 143067.
  108. Torii, S., Oishi, W., Zhu, W., Thakali, O., Malla, B., Yu, Z., Zhao, B., Arakawa C., Kitajima, M., Hata, A., Ihara, M., Kyuwa, S., Sano, D., Haramoto, E., and Katayama, H. (2022). Comparison of five polyethylene glycol precipitation procedures for the RT-qPCR based recovery of murine hepatitis virus, bacteriophage phi6, and pepper mild mottle virus as a surrogate for SARS-CoV-2 from wastewater, Science of the Total Environment, 807, 150722.
  109. Tran, H. N., Le, G. T., Nguyen, D. T., Juang, R. S., Rinklebe, J., Bhatnagar, A., Lima, E. C., Iqbal, H. M. N., Sarmah, A. K., Chao, H. P. (2021). SARS-CoV-2 coronavirus in water and wastewater: A critical review about presence and concern, Environmental Research, 193, 110265.
  110. Udugama, B., Kadhiresan, P., Kozlowski, H. N., Malekjahani, A., Osborne, M., Li, V. Y. C., Chen, H., Mubareka, S., Gubbay, J. B., and Chan, W. C. W. (2020). Diagnosing COVID-19: The Disease and Tools for Detection, ACS Nano, 14(4), 3822-3835. https://doi.org/10.1021/acsnano.0c02624
  111. Westhaus, S., Weber, F., Schiwy, S., Linnemann, V., Brinkmann, M., Widera, M., Greve, C., Janke, A., Hollert, H., Wintgens, T., and Ciesek, S. (2021). Detection of SARS-CoV-2 in raw and treated wastewater in Germany - Suitability for COVID-19 surveillance and potential transmission risks, Science of the Total Environment, 751, 141750.
  112. Wolters, F., van de Bovenkamp, J., van den Bosch, B., van den Brink, S., Broeders, M., Chung N., H., Favie, B., Goderski, G., Kuijpers, J., Overdevest, I., Rahamat-Langedoen, J., Wijsman, L., Melchers, W., J., and Meijer, A. (2020). Multicenter evaluation of cepheid xpert xpress SARS-CoV-2 point-of-care test during the SARS-CoV-2 pandemic, Journal of Clinical Virology, 128, 104426.
  113. World Health Organization (WHO). (2022). WHO coronavirus disease (COVID-19), Dashboard. https://covid19.who.int/. (accessed December 2022).
  114. Wu, F., Zhang, J., Xiao, A., Gu, X., Lee, W. L., Armas, F., Kauffman, K., Hanage, W., Matus, M., Ghaeli, N., Endo, N., Duvallet, C., Poyet, M., Moniz, K., Washburne, A. D., Erickson, T. B., Chai, P. R., Thompson, J., and Alm, E. J. (2020). SARS-CoV-2 titers in wastewater are higher than expected from clinically confirmed cases, ASM Journal, mSystems, e00614-20.
  115. Wurtzer, S., Marechal, V., Mouchel, J., Maday, Y., Teyssou, R., Richard, E., Almayrac, J., and Moulin, L. (2020). Evaluation of lockdown impact on SARS-CoV-2 dynamics through viral genome quantifcation in wastewater, Greater Paris, France, 5 March to 23 April 2020. medRxiv.
  116. Yu, L., Wu, S., Hao, X., Dong, X., Mao, L., Pelechano, V., Chen, W. H., and Yin, X. (2020). Rapid detection of COVID-19 coronavirus using a reverse transcriptional loop-mediated isothermal amplification (RT-LAMP) diagnostic platform, Clinical Chemistry, 66(7), 975-977. https://doi.org/10.1093/clinchem/hvaa102
  117. Zhang, D., Ling, H., Huang, X., Li, J., Li, W., Yi, C., Zhang, T., Jiang, Y., He, Y., Deng, S., Zhang, X., Wang, X., Liu, Y., Li, G., and Qu, J. (2020). Potential spreading risks and disinfection challenges of medical wastewater by the presence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) viral RNA in septic tanks of Fangcang Hospital, Science of the Total Environment, 741, 140445.
  118. Zhang, Y., Odiwuor, N., Xiong, J., Sun, L., Nyaruaba, R. O., Wei H., and Tanner N. A. (2020). Rapid molecular detection of SARS-CoV-2 (COVID-19) virus RNA using colorimetric LAMP, MedRxiv, 2020.02.26.20028373. 2020
  119. Zhen, W., Smith, E., Manji, R., Schron, D., and Berry, G., J. (2020). Clinical evaluation of three sample-to-answer platforms for the detection of SARS-CoV-2, Journal of Clinical Microbiology, 58(8), e00783-20.