Abstract
This study assessed wastewater quality through the quantification of four human enteric viruses and the applicability of pepper mild mottle virus (PMMoV) and tobacco mosaic virus (TMV) as indicators of viral reduction during wastewater treatment. Thirty-three samples were collected from three steps of a wastewater treatment plant in Southern Louisiana, USA for a year between March 2017 and February 2018. Noroviruses of genogroup I were the most prevalent human enteric viruses in influent samples. The concentrations of PMMoV in influent samples (5.9 ± 0.7 log10 copies/L) and biologically treated effluent samples (5.9 ± 0.5 log10 copies/L) were significantly higher than those of TMV (P < 0.05), and the reduction ratio of PMMoV (1.0 ± 0.8 log10) was found comparable to those of TMV and Aichi virus 1. Because of the high prevalence, high correlations with human enteric viruses, and lower reduction ratios, PMMoV was deemed an appropriate indicator of human enteric viral reduction during wastewater treatment process.
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References
Balique, F., Colson, P., Barry, A. O., Nappez, C., Ferretti, A., Moussawi, K. A., et al. (2013). Tobacco mosaic virus in the lungs of mice following intra-tracheal inoculation. PLoS ONE, 8, 1–12. https://doi.org/10.1371/journal.pone.0054993.
Bibby, K., Crank, K., Greaves, J., Li, X., Wu, Z., & Hamza, I. A. (2019). Metagenomics and the development of viral water quality tools. NPJ Clean Water, 2, 9. https://doi.org/10.1038/s41545-019-0032-3.
Bofill-Mas, S., Albinana-Gimenez, N., Clemente-Casares, P., Hundesa, A., Rodriguez-Manzano, J., Allard, A., et al. (2006). Quantification and stability of human adenoviruses and polyomavirus JCPyV in wastewater matrices. Applied Environmental Microbiology, 72(12), 7894–7896. https://doi.org/10.1128/AEM.00965-06.
Campos, C. J. A., Avant, J., Lowther, J., Till, D., & Lees, D. N. (2016). Human norovirus in untreated sewage and effluents from primary, secondary and tertiary treatment processes. Water Research, 103, 224–232. https://doi.org/10.1016/j.watres.2016.07.045.
Carratalà, A., Rusinol, M., Hundesa, A., Biarnes, M., Rodriguez-Manzano, J., Vantarakis, A., et al. (2012). A novel tool for specific detection and quantification of chicken/turkey parvoviruses to trace poultry fecal contamination in the environment. Applied Environmental Microbiology, 78, 7496–7499. https://doi.org/10.1128/AEM.01283-12.
da Silva, A. K., Le Saux, J. C., Parnaudeau, S., Pommepuy, M., Elimelech, M., & Le Guyader, F. S. (2007). Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: Different behaviors of genogroups I and II. Applied Environmental Microbiology, 73, 7891–7897. https://doi.org/10.1128/AEM.01428-07.
Eftim, S. E., Hong, T., Soller, J., Boehm, A., Warren, I., Ichida, A., et al. (2017). Occurrence of norovirus in raw sewage: A systematic literature review and meta-analysis. Water Research, 111, 366–374. https://doi.org/10.1016/j.watres.2017.01.017.
Fong, T. T., Phanikumar, M. S., Xagoraraki, I., & Rose, J. B. (2010). Quantitative detection of human adenoviruses in wastewater and combined sewer overflows influencing a Michigan River. Applied Environmental Microbiology, 76, 715–723. https://doi.org/10.1128/AEM.01316-09.
Fumian, T. M., Fioretti, J. M., Lun, J. H., Dos Santos, I. A. L., White, P. A., & Miagostovich, M. P. (2019). Detection of norovirus epidemic genotypes in raw sewage using next generation sequencing. Environment International, 123, 282–291. https://doi.org/10.1016/j.envint.2018.11.054.
Gerba, C. P., Betancourt, W. Q., Kitajima, M., & Rock, C. M. (2018). Reducing uncertainty in estimating virus reduction by advanced water treatment processes. Water Research, 133, 282–288. https://doi.org/10.1016/j.watres.2018.01.044.
Hamza, I. A., Jurzik, L., Uberla, K., & Wilhelm, M. (2011). Evaluation of pepper mild mottle virus, human picobirnavirus and torque teno virus as indicators of fecal contamination in river water. Water Research, 45, 1358–1368. https://doi.org/10.1016/j.watres.2010.10.021.
Haramoto, E., Fujino, S., & Otagiri, M. (2015). Distinct behaviors of infectious F-specific RNA coliphage genogroups at a wastewater treatment plant. Science of the Total Environment, 520, 32–38. https://doi.org/10.1016/j.scitotenv.2015.03.034.
Haramoto, E., Katayama, H., Oguma, K., & Ohgaki, S. (2007). Quantitative analysis of human enteric adenoviruses in aquatic environments. Journal of Applied Microbiology, 103, 2153–2159. https://doi.org/10.1111/j.1365-2672.2007.03453.x.
Haramoto, E., Katayama, H., Oguma, K., Yamashita, H., Tajima, A., Nakajima, H., et al. (2006). Seasonal profiles of human noroviruses and indicator bacteria in wastewater treatment plant in Tokyo, Japan. Water Science and Technology, 54, 301–308.
Haramoto, E., Kitajima, M., Hata, A., Torrey, J. R., Masago, Y., Sano, D., et al. (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.
Hata, A., Kitajima, M., & Katayama, H. (2013). Occurrence and reduction of human viruses, F-specific RNA coliphage genogroups and microbial indicators at a full-scale wastewater treatment plant in Japan. Journal of Applied Microbiology, 114, 545–554. https://doi.org/10.1111/jam.12051.
Hewitt, J., Greening, G. E., Leonard, M., & Lewis, G. D. (2013). Evaluation of human adenovirus and human polyomavirus as indicators of human sewage contamination in the aquatic environment. Water Research, 47, 6750–6761. https://doi.org/10.1016/j.watres.2013.09.001.
Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., et al. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of Clinical Microbiology, 41, 1548–1557. https://doi.org/10.1128/jcm.41.4.1548-1557.2003.
Katayama, H., Haramoto, E., Oguma, K., Yamashita, H., Tajima, A., Nakajima, H., et al. (2008). One-year monthly quantitative survey of noroviruses, enteroviruses, and adenoviruses in wastewater collected from six plants in Japan. Water Research, 42, 1441–1448. https://doi.org/10.1016/j.watres.2007.10.029.
Katayama, H., Shimasaki, A., & Ohgaki, S. (2002). Development of a virus concentration method and its application to detection of enterovirus and Norwalk virus from coastal seawater. Applied Environmental Microbiology, 68, 1033–1039. https://doi.org/10.1128/aem.68.3.1033-1039.2002.
Kitajima, M., Haramoto, E., Phanuwan, C., & Katayama, H. (2011). Prevalence and genetic diversity of Aichi viruses in wastewater and river water in Japan. Applied Environmental Microbiology, 77, 2184–2187. https://doi.org/10.1128/AEM.02328-10.
Kitajima, M., Iker, B. C., Pepper, I. L., & Gerba, I. L. (2014). Relative abundance and treatment reduction of viruses during wastewater treatment processes identification of potential viral indicators. Science of the Total Environment, 488, 290–296. https://doi.org/10.1016/j.scitotenv.2014.04.087.
Kitajima, M., Sassi, H. P., & Torrey, J. R. (2018). Pepper mild mottle virus as a water quality indicator. NPJ Clean Water, 1, 19. https://doi.org/10.1038/s41545-018-0019-5.
Ottoson, J., Hansen, A., Björlenius, B., Norder, H., & Stenström, T. A. (2006). Removal of viruses, parasitic protozoa and microbial indicators in conventional and membrane processes in a wastewater pilot plant. Water Research, 40, 1449–1457.
Qiu, Y., Lee, B. E., Neumann, N., Ashbolt, N., Craik, S., Maal-Bared, R., et al. (2015). Assessment of human virus removal during municipal wastewater treatment in Edmonton, Canada. Journal of Applied Microbiology, 119, 1729–1739. https://doi.org/10.1111/jam.12971.
Savichtcheva, O., & Okabe, S. (2006). Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Research, 40, 2463–2476.
Schmitz, B. W., Kitajima, M., Campillo, M. E., Gerba, C. P., & Pepper, I. L. (2016). Virus reduction during advanced bardenpho and conventional wastewater treatment processes. Environmental Science and Technology, 50, 9524–9532. https://doi.org/10.1021/acs.est.6b01384.
Shieh, Y. S., Wait, D., Tai, L., & 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, 51–66.
Shrestha, S., Shrestha, S., Shindo, J., Sherchand, J. B., & Haramoto, E. (2018). Virological quality of irrigation water sources and pepper mild mottle virus and tobacco mosaic virus as index of pathogenic virus contamination level. Food Environmental Virology, 10, 107–120. https://doi.org/10.1007/s12560-017-9324-2.
Tandukar, S., Sherchand, S. P., & Haramoto, E. (2020). Applicability of crAssphage, pepper mild mottle, and tobacco mosaic virus as indicators of reduction of enteric viruses during wastewater treatment. Scientific Reports, 10, 3616.
Wood, M. D., Beresford, N. A., & Copplestone, D. (2011). Limit of detection values in data analysis: Do they matter? Radioprotection, 46, S85–S90. https://doi.org/10.1051/radiopro/20116728s.
Zhang, T., Breitbart, M., Lee, W. H., Run, J. Q., Wei, C. L., Soh, S. W., et al. (2005). RNA viral community in human feces: Prevalence of plant pathogenic viruses. PLOS Biology, 4, 108–118. https://doi.org/10.1371/journal.pbio.0040003.
Acknowledegment
This study was partially supported by the Japan Society for the Promotion of Science through Grant-in-Aid for Scientific Research (B) (Grant Number JP17H03332) and by the Board of Regents grant number LEQSF (2018-21)-rd-a-21 to Dr. Samendra Sherchan. The authors thank Dr. Jia Xue and Mr. Collin Potter (Tulane University, USA), and Dr. Bikash Malla, Dr. Rajani Ghaju Shrestha, Mr. Ocean Thakali, Ms. Niva Sthapit, and Mr. Bijay Man Shakya (University of Yamanashi, Japan).
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Tandukar, S., Sherchan, S.P. & Haramoto, E. Reduction of Human Enteric and Indicator Viruses at a Wastewater Treatment Plant in Southern Louisiana, USA. Food Environ Virol 12, 260–263 (2020). https://doi.org/10.1007/s12560-020-09433-1
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DOI: https://doi.org/10.1007/s12560-020-09433-1