Abstract
Roof-harvested rainwater (RHRW) is considered relatively clean water, even though the possible presence of pathogens in the water may pose human health risks. In this study, we investigated the occurrence of enteric viruses in the first flush (10 mm) of RHRW from a densely populated and low-income urbanized region of Rio de Janeiro. One hundred samples (5 L) were collected from 10 rainfall events between April 2015 and March 2017. RNA and DNA viruses were concentrated using the skimmed milk flocculation method and analyzed using the TaqMan® quantitative RT-qPCR and qPCR. Human adenoviruses, noroviruses, rotaviruses A, and avian parvoviruses were detected in 54%, 31%, 12%, and 12% of the positive samples. JC polyomavirus, also targeted, was not detected. Virus concentrations ranged from 1.09 × 101 to 2.58 × 103 genome copies/Liter (GC/L). Partial nucleotide sequence confirmed the presence of HAdV type 41, norovirus genotype GII.4, and avian parvovirus 1. The results suggest that the first flush diversion devices may not adequately remove enteric virus from the rainwater. Additional treatment of RHRW is required to mitigate potential health risks from potable use of captured water.
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References
Ahmed, W., Goonetilleke, A., & Gardner, T. (2010). Implications of faecal indicator bacteria for the microbiological assessment of roof-harvested rainwater quality in southeast Queensland, Australia. Canadian Journal of Microbiology, 56, 471–479. https://doi.org/10.1139/w10-037
Ahmed, W., Gardner, T., & Toze, S. (2011). Microbiological quality of roof-harvested rainwater and health risks: A review. Journal of Environmental Quality, 40, 13–21. https://doi.org/10.2134/jeq2010.0345
Ahmed, W., Hodgers, L., Sidhu, J., Gardner, T., Richardson, K., Palmer, A., et al. (2012). Health risk assessment of roof-captured rainwater [Internet]. Australia: Commonwealth Scientific and Industrial Research Organization - CSIRO; p. 76. Report No.: 77. Available at https://publications.csiro.au/rpr/download?pid=csiro:EP128414&dsid=DS4
Ahmed, W., Gyawali, P., Sidhu, J. P. S., & Toze, S. (2014). Relative inactivation of faecal indicator bacteria and sewage markers in freshwater and seawater microcosms. Letters in Applied Microbiology, 59, 348–354. https://doi.org/10.1111/lam.12285
Ahmed, W., Hamilton, K., Toze, S., Cook, S., & Page, D. (2019). A review on microbial contaminants in stormwater runoff and outfalls: Potential health risks and mitigation strategies. Science of The Total Environment, 692, 1304–1321. https://doi.org/10.1016/j.scitotenv.2019.07.055
Allard, A., Albinsson, B., Wadell, G. (2001). Rapid typing of human adenoviruses by a general PCR combined with restriction endonuclease analysis. Journal of Clinical Microbiology, 39(2), 498–505. https://doi.org/10.1128/JCM.39.2.498-505.2001
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Assis, A. S. F., Fumian, T. M., Miagostovich, M. P., Drumond, B. P., & e Silva, M. L. D. R. (2018). Adenovirus and rotavirus recovery from a treated effluent through an optimized skimmed-milk flocculation method. Environmental Science and Pollution Research, 25, 17025–17032. https://doi.org/10.1007/s11356-018-1873-x
Bae, S., Maestre, J. P., Kinney, K. A., & Kirisits, M. J. (2019). An examination of the microbial community and occurrence of potential human pathogens in rainwater harvested from different roofing materials. Water Research, 159, 406–413. https://doi.org/10.1016/j.watres.2019.05.029
Bofill-Mas, S., Rusiñol, M., Fernandez-Cassi, X., Carratalà, A., Hundesa, A., & Girones, R. (2013). Quantification of human and animal viruses to differentiate the origin of the fecal contamination present in environmental samples. BioMed Research International. https://doi.org/10.1155/2013/192089
Calgua, B., Fumian, T. M., Rusiñol, M., Rodriguez-Manzano, J., Mbayed, V. A., Bofill-Mas, S., Miagostovich, M., & Girones, R. (2013). Detection and quantification of classic and emerging viruses by skimmed-milk flocculation and PCR in river water from two geographical areas. Water Research, 47, 2797–2810. https://doi.org/10.1016/j.watres.2013.02.043
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 and Environmental Microbiology, 78(20), 7496–7499. https://doi.org/10.1128/AEM.01283-12
Chidamba, L., & Korsten, L. (2015). Pyrosequencing analysis of roof-harvested rainwater and river water used for domestic purposes in Luthengele village in the Eastern Cape Province of South Africa. Environmental Monitoring and Assessment, 187, 41. https://doi.org/10.1007/s10661-014-4237-0
Chubaka, C. E., Whiley, H., Edwards, J. W., & Ross, K. E. (2018). Microbiological values of rainwater harvested in Adelaide. Pathogens (Basel, Switzerland). https://doi.org/10.3390/pathogens7010021
de Kwaadsteniet, M., Dobrowsky, P. H., van Deventer, A., Khan, W., & Cloete, T. E. (2013). Domestic rainwater harvesting: Microbial and chemical water quality and point-of-use treatment systems. Water, Air, & Soil Pollution, 224, 1629. https://doi.org/10.1007/s11270-013-1629-7
DeBusk, K., Hunt, W. Rainwater harvesting: A comprehensive review of literature [Internet]. Water Resources Research Institute of the University of North Carolina; 2014. Report No.: 425. Available at http://www.lib.ncsu.edu/resolver/1840.4/8170
Evans, C. A., Coombes, P. J., & Dunstan, R. H. (2006). Wind, rain and bacteria: The effect of weather on the microbial composition of roof-harvested rainwater. Water Research, 40, 37–44. https://doi.org/10.1016/j.watres.2005.10.034
Ferreira, F. F. M., Guimarães, F. R., Fumian, T. M., Victoria, M., Vieira, C. B., Luz, S., Shubo, T., Leite, J. P. G., & Miagostovich, M. P. (2009). Environmental dissemination of group A rotavirus: P-type, G-type and subgroup characterization. Water Science and Technology, 60, 633–642. https://doi.org/10.2166/wst.2009.413
Fumian, T. M., Guimarães, F. R., Pereira Vaz, B. J., da Silva, M. T. T., Muylaert, F. F., Bofill-Mas, S., Gironés, R., Leite, J. P. G., & Miagostovich, M. P. (2010). Molecular detection, quantification and characterization of human polyomavirus JC from waste water in Rio De Janeiro, Brazil. Journal of Water and Health, 8, 438–445. https://doi.org/10.2166/wh.2010.090
Fumian, T. M., Gagliardi Leite, J. P., Rose, T. L., Prado, T., & Miagostovich, M. P. (2011). One year environmental surveillance of rotavirus specie A (RVA) genotypes in circulation after the introduction of the Rotarix® vaccine in Rio de Janeiro, Brazil. Water Research, 45, 5755–5763. https://doi.org/10.1016/j.watres.2011.08.039
Fumian, T. M., Fioretti, J. M., Lun, J. H., Dos Santos, I. A., 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
Gikas, G. D., & Tsihrintzis, V. A. (2012). Assessment of water quality of first-flush roof runoff and harvested rainwater. Journal of Hydrology, 466–467, 115–126. https://doi.org/10.1016/j.jhydrol.2012.08.020
Gikas, G. D., & Tsihrintzis, V. A. (2017). Effect of first-flush device, roofing material, and antecedent dry days on water quality of harvested rainwater. Environmental Science and Pollution Research, 24, 21997–22006. https://doi.org/10.1007/s11356-017-9868-6
Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment and analysis program for Windows 95/98/NT. In: Nucleic Acids Symposium Series (pp. 95–98)
Hamilton, K., Reyneke, B., Waso, M., Clements, T., Ndlovu, T., Khan, W., DiGiovanni, K., Rakestraw, E., Montalto, F., Haas, C. N., & Ahmed, W. (2019). A global review of the microbiological quality and potential health risks associated with roof-harvested rainwater tanks. NPJ Clean Water, 2, 1–18. https://doi.org/10.1038/s41545-019-0030-5
Handam, N. B., dos Santos, J. A. A., de Moraes Neto, A. H. A., Duarte, A. N., Alves, E. B. D. S., Salles, M. J., & Sotero-Martins, A. (2018). Sanitary quality of the rivers in the Communities of Manguinhos´ Territory, Rio de Janeiro, RJ. Revista Ambiente & Água. https://doi.org/10.4136/ambi-agua.2125
Harwood, V. J., Staley, C., Badgley, B. D., Borges, K., & Korajkic, A. (2014). Microbial source tracking markers for detection of fecal contamination in environmental waters: Relationships between pathogens and human health outcomes. FEMS Microbiology Reviews, 38, 1–40. https://doi.org/10.1111/1574-6976.12031
Hernroth, B. E., Conden-Hansson, A. C., Rehnstam-Holm, A. S., Girones, R., & Allard, A. K. (2002). Factors influencing human viral pathogens and their potential indicator organisms in the blue mussel, Mytilus edulis: the first Scandinavian report. Applied and Environmental Microbiology, 68(9), 4523–4533. https://doi.org/10.1128/AEM.68.9.4523-4533.2002
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
Jongman, M., & Korsten, L. (2016). Microbial quality and suitability of roof-harvested rainwater in rural villages for crop irrigation and domestic use. Journal of Water and Health, 14, 961–971. https://doi.org/10.2166/wh.2016.058
Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., Takeda, N., Katayama, K. (2003). Broadly reactive and highly sensitive assay for norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of Clinical Microbiology, 41(4), 1548–1557. https://doi.org/10.1128/JCM.41.4.1548-1557.2003
Kim, T., Lye, D., Donohue, M., Mistry, J. H., Pfaller, S., Vesper, S., & Kirisits, M. J. (2016). Harvested rainwater quality before and after treatment and distribution in residential systems. Journal-American Water Works Association, 108, E571–E584. https://doi.org/10.5942/jawwa.2016.108.0182
Kojima, S., Kageyama, T., Fukushi, S., Hoshino, F. B., Shinohara, M., Uchida, K., Natori, K., Takeda, N., & Katayama, K. (2002). Genogroup-specific PCR primers for detection of Norwalk-like viruses. Journal of Virological Methods, 100(1–2), 107–114. https://doi.org/10.1016/S0166-0934(01)00404-9
Kus, B., Kandasamy, J., Vigneswaran, S., & Shon, H. K. (2010). Analysis of first flush to improve the water quality in rainwater tanks. Water Science and Technology, 61, 421–428. https://doi.org/10.2166/wst.2010.823
Lo, A. G., & Gould, J. (2015). Rainwater harvesting: Global overview. In Q. Zhu, J. Gould, Y. Li, & C. Ma (Eds.), Rainwater harvesting for agriculture and water supply (pp. 213–233). Springer Singapore.
Magalhães, R., Coelho, A. V., Nogueira, M. F., & Bocca, C. (2011). Intersetorialidade, convergência e sustentabilidade: desafios do programa Bolsa Família em Manguinhos, RJ. Ciência & Saúde Coletiva, 16, 4442–4453. https://doi.org/10.1590/S1413-81232011001200017
Mekonnen, M. M., & Hoekstra, A. Y. (2016). Four billion people facing severe water scarcity. Science Advances, 2, e1500323. https://doi.org/10.1126/sciadv.1500323
Pal, A., Sirota, L., Maudru, T., Peden, K., & Lewis, A. M. (2006). Real-time quantitative PCR assays for the detection of virus-specific DNA in samples with mixed populations of polyomaviruses. Journal of Virological Methods, 135(1), 32–42. https://doi.org/10.1016/j.jviromet.2006.01.018
Piqueras, P., Li, F., Castelluccio, V., Matsumoto, M., & Asa-Awuku, A. (2016). Real-time ultrafine aerosol measurements from wastewater treatment facilities. Environmental Science & Technology, 50, 11137–11144. https://doi.org/10.1021/acs.est.6b02684
Qomariyah, S. (2016). Decentralized system of greywater recycling for sustainable urban water source (Case Study: Surakarta City-Indonesia). In: Appl. Mech. Mater./AMM.845.18. Accessed 19 May 2020.
Rajal, V. B., McSwain, B. S., Thompson, D. E., Leutenegger, C. M., Kildare, B. J., & Wuertz, S. (2007). Validation of hollow fiber ultrafiltration and real-time PCR using bacteriophage PP7 as surrogate for the quantification of viruses from water samples. Water Research, 41, 1411–1422. https://doi.org/10.1016/j.watres.2006.12.034
Sánchez, A. S., Cohim, E., & Kalid, R. A. (2015). A review on physicochemical and microbiological contamination of roof-harvested rainwater in urban areas. Sustainability of Water Quality and Ecology, 6, 119–137. https://doi.org/10.1016/j.swaqe.2015.04.002
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. https://doi.org/10.1016/j.watres.2006.04.040
Schets, F. M., Italiaander, R., van den Berg, H. H. J. L., & de Roda Husman, A. M. (2010). Rainwater harvesting: Quality assessment and utilization in The Netherlands. Journal of Water and Health, 8, 224–235. https://doi.org/10.2166/wh.2009.037
Sidhu, J. P. S., Sena, K., Hodgers, L., Palmer, A., & Toze, S. (2018). Comparative enteric viruses and coliphage removal during wastewater treatment processes in a sub-tropical environment. Science of the Total Environment, 616–617, 669–677. https://doi.org/10.1016/j.scitotenv.2017.10.265
Silva Vieira, A., Weeber, M., & Ghisi, E. (2013). Self-cleaning filtration: A novel concept for rainwater harvesting systems. Resources, Conservation and Recycling, 78, 67–73. https://doi.org/10.1016/j.resconrec.2013.06.008
Sistema Alerta Rio Dados Pluviométricos. http://www.sistema-alerta-rio.com.br/dados-meteorologicos/download/dados-pluviometricos/. Accessed 11 Aug 2020.
Staggemeier, R., Heck, T. M. S., Demoliner, M., Ritzel, R. G., Röhnelt, N. M., Girardi, V., Venker, C. A., & Spilki, F. R. (2017). Enteric viruses and adenovirus diversity in waters from 2016 Olympic venues. Science of the Total Environment, 586, 304–312. https://doi.org/10.1016/j.scitotenv.2017.01.223
UNCCD. (2014). Desertification: The Invisible Frontline. https://www.unccd.int/publications/desertification-invisible-frontline-second-edition. Accessed 4 Oct 2020.
Vergara, G. G. R. V., Rose, J. B., & Gin, K. Y. H. (2016). Risk assessment of noroviruses and human adenoviruses in recreational surface waters. Water Research, 103, 276–282. https://doi.org/10.1016/j.watres.2016.07.048
Victoria, M., Guimarães, F. R., Fumian, T. M., Ferreira, F. F. M., Vieira, C. B., Shubo, T., Leite, J. P. G., & Miagostovich, M. P. (2009). One year monitoring of norovirus in a sewage treatment plant in Rio de Janeiro, Brazil. Journal of Water and Health, 8, 158–165. https://doi.org/10.2166/wh.2009.012
Waso, M., Ndlovu, T., Dobrowsky, P. H., Khan, S., & Khan, W. (2016). Presence of microbial and chemical source tracking markers in roof-harvested rainwater and catchment systems for the detection of fecal contamination. Environmental Science and Pollution Research, 23, 16987–17001. https://doi.org/10.1007/s11356-016-6895-7
Xavier, R. P., Siqueira, L. P., Vital, F. A. C., Rocha, F. J. S., Irmão, J. I., & Calazans, G. M. T. (2011). Microbiological quality of drinking rainwater in the inland region of Pajeú, Pernambuco, Northeast Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 53, 121–124. https://doi.org/10.1590/S0036-46652011000300001
Zeng, S.-Q., Halkosalo, A., Salminen, M., Szakal, E. D., Puustinen, L., & Vesikari T. (2008). One-step quantitative RT-PCR for the detection of rotavirus in acute gastroenteritis. Journal of Virological Methods, 153(2), 238–240. https://doi.org/10.1016/j.jviromet.2008.08.004
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We would like to thank Mr. Roger DaSilva for helping with the English review. This research work is within the scope of the activities of FIOCRUZ as a collaborating center of PAHO/WHO of Public and Environmental Health.
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Marize Pereira Miagostovich is a CNPq fellow and got funding from CNPq (National Council of Technological and Scientific Development); SVS—Ministry of Health n° 015/2015; and PAEF 2—Instituto Oswaldo Cruz.
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All authors critically revised the article for important intellectual content and approved all components of the final draft. TS contributed with performing, developing, and designing the sampling methodology, field data collection, visualization of data, and writing the original draft; FCF and MMAP performed the concentration processes of the samples; AM performed molecular techniques: TMF performed the sequencing analysis; ST, WA, and JS reviewed the manuscript and provide scientific insights; CdRVM reviewed the manuscript; MPM contributed with the supervision, project management and financing acquisition.
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Shubo, T., Maranhão, A., Ferreira, F.C. et al. Virological Characterization of Roof-Harvested Rainwater of Densely Urbanized Low-Income Region. Food Environ Virol 13, 412–420 (2021). https://doi.org/10.1007/s12560-021-09484-y
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DOI: https://doi.org/10.1007/s12560-021-09484-y