Skip to main content

Advertisement

Log in

Assessment and Evaluation of an Integrated Hybrid Anaerobic–Aerobic Sewage Treatment System for the Removal of Enteric Viruses

  • Original Paper
  • Published:
Food and Environmental Virology Aims and scope Submit manuscript

Abstract

The capability of a cost-effective and a small size decentralized pilot wastewater treatment plant (WWTP) to remove enteric viruses such as rotavirus, norovirus genogroup I (GGI), norovirus genogroup II (GGII), Hepatitis E virus (HEV), and adenovirus was studied. This pilot plant is an integrated hybrid anaerobic/aerobic setup which consisted of anaerobic sludge blanket (UASB), biological aerated filter (BAF), and inclined plate settler (IPS). Both the UASB and BAF are packed with a non-woven polyester fabric (NWPF). Results indicated that the overall log10 reductions of enteric viruses’ genome copies through the whole system were 3.1 ± 1, 3.3 ± 0.5, and 2.6 ± 0.9 log10 for rotavirus, norovirus GGI, and adenovirus, respectively. Reduction efficiency for both norovirus GGII and HEV after the different treatment steps could not be calculated because there were no significant numbers of positive samples for both viruses. The overall reduction of rotavirus infectious units through the whole system was 2.2 ± 0.8 log10 reduction which is very close to the overall log10 reduction of adenovirus infectious units through the whole system which was 2.1 ± 0.8 log10 reduction. There was no considerable difference in the removal efficiency for different rotavirus G and P types. Adenovirus 41 was the only type detected in the all positive samples. Although the pilot WWTP investigated is cost effective, has a small footprint, does not need a long distance network pipes, and easy to operate, its efficiency to remove enteric viruses is comparable with the conventional centralized WWTPs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abad, F. X., Pintó, R. M., Diez, J. M., & Bosch, A. (1994). Disinfection of human enteric viruses in water by copper and silver in combination with low levels of chlorine. Applied and Environment Microbiology, 60, 2377–2383.

    CAS  Google Scholar 

  • Abad, F. X., Pintó, R. M., Villena, C., Gajardo, R., & Bosch, A. (1997). Astrovirus survival in drinking water. Applied and Environment Microbiology, 63, 3119–3122.

    CAS  Google Scholar 

  • Abdo, S. M., Hetta, M. H., El-Senousy, W. M., Samhan, F. A., Salah El Din, R. A., & Ali, G. H. (2012). Antiviral activity of freshwater algae. Journal of Applied Pharmaceutical Science, 2, 21–25.

    Google Scholar 

  • Abou-Elela, S. I., Fawzy, M. E., & El-Gendy, A. S. (2015). Potential of using biological aerated filter as a post treatment for municipal wastewater. Ecological Engineering Journal, 84, 53–57.

    Article  Google Scholar 

  • Abou-Elela, S. I., Fawzy, M. E., Emam, W. M., & Ghazy, M. M. (2013). Decentralized domestic wastewater treatment using a novel hybrid up-flow anaerobic sludge blanket followed by sand filtration. International Journal of Ecology and Environmental Sciences, 4(1), 91–96.

    CAS  Google Scholar 

  • Abou-Elela, S. I., Hamdy, I. O., & El Monayeri, O. (2016a). Modeling and simulation of anaerobic/aerobic wastewater treatment system. International Journal of Environmental Science and Technology, 13(5), 1289–1298.

    Article  CAS  Google Scholar 

  • Abou-Elela, S. I., Harb, A. H., & Hellal, M. S. (2016b). Assessment of seasonal variations on the performance of P-UASB/BAF for municipal wastewater treatment. Desalination and Water Treatment Journal, 57, 17087–17094.

    CAS  Google Scholar 

  • Atmar, R. L., Opekun, A. R., Gilger, M. A., Estes, M. K., Crawford, S. E., Neill, F. H., et al. (2008). Norwalk virus shedding after experimental human infection. Emerging Infectious Diseases, 14, 1553–1557.

    Article  PubMed  PubMed Central  Google Scholar 

  • Baggi, F., Demarta, A., & Peduzzi, R. (2001). Persistence of viral pathogens and bacteriophages during sewage treatment: Lack of correlation with indicator bacteria. Research in Microbiology, 152, 743–751.

    Article  CAS  PubMed  Google Scholar 

  • Bosch, A. (2007). Human viruses in water (1st ed.). Amsterdam, Boston: Elsevier.

    Google Scholar 

  • Bosch, A., Diez, J. M., & Abad, F. X. (1993). Disinfection of human enteric viruses in water by copper: Silver and reduced levels of chlorine. Water Science & Technology, 27, 351–356.

    CAS  Google Scholar 

  • Breitbart, M., Hewson, I., Felts, B., Mahaffy, J. M., Nulton, J., Salamon, P., et al. (2003). Metagenomic analyses of an uncultured viral community from human feces. Journal of Bacteriology, 185, 6220–6223.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao, H., Tsai, F. T. C., & Rusch, K. A. (2010). Salinity and soluble organic matter on virus sorption in sand and soil columns. Ground Water, 48, 42–52.

    Article  CAS  PubMed  Google Scholar 

  • Cho, H. B., Lee, S. H., Cho, J. C., & Kim, S. J. (2000). Detection of adenoviruses and enteroviruses in tap water and river water by reverse transcription multiplex PCR. Canadian Journal of Microbiology, 46, 417–424.

    Article  CAS  PubMed  Google Scholar 

  • Costafreda, M. I., Bosch, A., & Pintó, R. M. (2006). Development, evaluation, and standardization of a real-time TaqMan reverse transcription-PCR assay for quantification of hepatitis a virus in clinical and shellfish samples. Applied and Environment Microbiology, 72(6), 3846–3855.

    Article  CAS  Google Scholar 

  • 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 and Environment Microbiology, 73(24), 7891–7897.

    Article  Google Scholar 

  • de Roda Husman, A. M., & Bartram, J. (2008). Global supply of virus safe drinking water. In A. Bosch (Ed.), Human viruses in water (pp. 127–162). Amsterdam: Elsevier.

    Google Scholar 

  • El-Senousy, W. M., Barakat, A. B., Ghanem, H. E., & Kamel, M. A. (2013a). Molecular epidemiology of human adenoviruses and rotaviruses as candidate viral indicators in the Egyptian sewage and water samples. World Applied Sciences Journal, 27, 1235–1247.

    Google Scholar 

  • El-Senousy, W. M., Costafreda, M. I., Pintó, R. M., & Bosch, A. (2013b). Method validation for norovirus detection in naturally contaminated irrigation water and fresh produce. International Journal of Food Microbiology, 167, 74–79.

    Article  CAS  PubMed  Google Scholar 

  • El-Senousy, W. M., El-Gamal, M. S., Mousa, A. A., El-Hawary, S. E., Kamel, M. M., Fathi, M. N., et al. (2014). Effect of chlorine on noroviruses, rotaviruses, and hepatitis E virus in drinking water. World Applied Sciences Journal, 32(11), 2206–2212.

    CAS  Google Scholar 

  • El-Senousy, W. M., Guix, S., Abid, I., Pintó, R. M., & Bosch, A. (2007). Removal of astrovirus from water and sewage treatment plants, evaluated by a competitive reverse transcription-PCR. Applied and Environment Microbiology, 73, 164–167.

    Article  CAS  Google Scholar 

  • Esawy, M. A., Ahmed, E. F., Helmy, W. A., Mansour, N. M., El-Senousy, W. M., & El-Safty, M. M. (2011). Production of a halophilic levansucrase from novel honey Bacillus subtilis isolates capable of producing antiviral levans. Carbohydrate Polymers, 86, 823–830.

    Article  CAS  Google Scholar 

  • Espinosa, A. C., Arias, C. F., Sánchez-Colón, S., & Mazari-Hiriart, M. (2009). Comparative study of enteric viruses, coliphages and indicator bacteria for evaluating water quality in a tropical high-altitude system. Environment Health, 8, 49–58.

    Article  Google Scholar 

  • Espinosa, A. C., Mazari-Hiriart, M., Espinosa, R., Maruri Avidal, L., Méndez, E., & Arias, F. C. (2008). Infectivity and genome persistence of rotavirus and astrovirus in groundwater and surface water. Water Research, 42, 2618–2628.

    Article  CAS  PubMed  Google Scholar 

  • Estrada, C. S. M. L., Velasquez, L. D. C., Genaro, S. D., & Guzman, A. M. S. D. (2007). Comparison of DNA extraction methods for pathogenic Yersinia enterocolitica detection from meat food by nested PCR. Food Research International, 40, 637–642.

    Article  Google Scholar 

  • Gallimore, C. I., Taylor, C., Genney, A. R., Cant, A. J., Galloway, A., Iturriza-Gomara, M., et al. (2006). Environmental monitoring for gastroenteric viruses in a pediatric primary immunodeficiency unit. Journal of Clinical Microbiology, 44, 395–399.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gantzer, C., Maul, A., Audic, J. M., & Schwartzbrod, L. (1998). Detection of infectious enteroviruses, enterovirus genomes, somatic coliphages, and Bacteroides fragilis phages in treated wastewater. Applied and Environment Microbiology, 64, 4307–4312.

    CAS  Google Scholar 

  • Gentsch, J. R., Glass, R. I., Woods, P. V., Gouvea, V., Gorziglia, M., Flores, J., et al. (1992). Identification of group A rotavirus gene 4 types by polymerase chain reaction. Journal of Clinical Microbiology, 30, 1365–1373.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gerba, C. P., Gramos, D. M., & Nwachuku, N. (2002). Comparative inactivation of enteroviruses and adenovirus 2 by UV light. Applied and Environment Microbiology, 68, 5167–5169.

    Article  CAS  Google Scholar 

  • Gerba, C. P., & Rose, J. B. (1990). Viruses in source and drinking water. In G. A. McFeters (Ed.), Drinking water microbiology: Progress and recent developments (pp. 380–396). New York (NY): Springer-Verlag.

    Chapter  Google Scholar 

  • Ghazy, M. M. E., El-Senousy, W. M., Abdel- Aatty, A. M., Hegazy, B., & Kamel, M. (2008). Performance evaluation of a waste stabilization pond in a rural area in Egypt. American Journal of Environmental Sciences, 4, 316–326.

    Article  Google Scholar 

  • Gouvea, V., Glass, R. I., Woods, P., Taniguchi, K., Clark, H. F., Forrester, B., et al. (1990). Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. Journal of Clinical Microbiology, 28, 276–282.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gouvea, V., Santos, N., & Carmo Timenetsky, M. (1994a). Identification of bovine and porcine rotavirus G types by PCR. Journal of Clinical Microbiology, 32, 1338–1340.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gouvea, V., Santos, N., & Carmo Timenetsky, M. (1994b). VP4 typing of bovine and porcine group A rotavirus by PCR. Journal of Clinical Microbiology, 32, 1333–1337.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Greninger, A., Runckel, C., Chiu, C., Haggerty, T., Parsonnet, J., Ganem, D., et al. (2009). The complete genome of Klassevirus - a novel picornavirus in pediatric stool. Virology Journal, 6, 82–90.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hao, X. D., Wang, Q. L., Zhu, J. Y., & Van Loosdrecht, M. C. M. (2010). Microbiological endogenous processes in biological wastewater treatment systems. Critical Reviews in Environment Science and Technology, 40, 239–265.

    Article  CAS  Google Scholar 

  • Hauri, A. M., Schimmelpfennig, M., Walter-Domes, M., Letz, A., Diedrich, S., Lopez-Pila, J., et al. (2005). An outbreak of viral meningitis associated with a public swimming pond. Epidemiology and Infection, 133, 291–298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Havelaar, A. H., van Olphen, M., & Drost, Y. C. (1993). F-specific RNA bacteriophages are adequate model organisms for enteric viruses in fresh water. Applied and Environment Microbiology, 59, 2956–2962.

    CAS  Google Scholar 

  • Iturriza Gomara, M., Wong, C., Blome, S., Desselberger, U., & Gray, J. (2002). Molecular characterization of VP6 genes of human rotavirus isolates: Correlation of genogroups with subgroups and evidence of independent segregation. Journal of Virology, 76, 6596–6601.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jothikumar, N., Aparna, K., Kamatchiammal, S., Paulmurugan, R., Saravanadevi, S., & Khanna, P. (1993). Detection of hepatitis E virus in raw and treated wastewater. Environmental Microbiology, 59, 2558–2562.

    CAS  Google Scholar 

  • Jurzik, L., Hamzaa, I. A., Puchert, W., Überla, K., & Wilhelm, M. (2010). Chemical and microbiological parameters as possible indicators for human enteric viruses in surface water. International Journal of Hygiene and Environmental Health, 213, 210–216.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapperud, G., Vardnund, T., Skjerve, E., Hornes, E., & Michaelsen, T. E. (1993). Detection of pathogenic Yersinia enterocolitica in foods and water by immunomagnetic separation, nested polymerase chain reaction and colorimetric detection of amplified DNA. Applied and Environment Microbiology, 59, 2938–2944.

    CAS  Google Scholar 

  • Kasorndorkbua, C., Opriessnig, T., Huang, F. F., Guenette, D. K., Thomas, P. J., Meng, X. J., et al. (2005). Infectious swine hepatitis E virus present in pig manure storage facilities on United States farms, but evidence of water contamination is lacking. Applied and Environment Microbiology, 71, 7831–7837.

    Article  CAS  Google Scholar 

  • Kitajima, M., Iker, B. C., Pepper, I. L., & Gerba, C. P. (2014). Relative abundance and treatment reduction of viruses during wastewater treatment processes—identification of potential viral indicators. Science of the Total Environment, 489, 290–296.

    Article  Google Scholar 

  • Kojima, S., Kageyama, T., Fukuda, S., Hoshino, F., Shinohara, M., Uchida, K., et al. (2002). Genogroup-specific PCR primer for detection of Norwalk-like viruses. Journal of Virological Methods, 100, 107–114.

    Article  CAS  PubMed  Google Scholar 

  • Le Guyader, F. S., Parnaudeau, S., Schaeffer, J., Bosch, A., Loisy, F., Pommepuy, M., et al. (2009). Detection and quantification of noroviruses in shellfish. Applied and Environment Microbiology, 75, 618–624.

    Article  Google Scholar 

  • Lewis, G. D., & 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 Environment Microbiology, 54, 1983–1988.

    CAS  Google Scholar 

  • Loisy, F., Atmar, R. L., Guillon, P., Le Cann, P., Pommepuy, M., & Le Guyader, F. S. (2005). Real-time RT-PCR for norovirus screening in shellfish. Journal of Virological Methods, 123(1), 1–7.

    Article  CAS  PubMed  Google Scholar 

  • Miagostovich, M. P., Ferreira, F. F., Guimaraes, F. R., Fumian, T. M., Diniz-Mendes, L., Luz, S. L., et al. (2004). The challenge of emerging and re-emerging infectious diseases. Nature, 430, 242–249.

    Article  Google Scholar 

  • Pintó, R. M., Costafreda, M. I., & Bosch, A. (2009). Risk assessment in shellfish-borne outbreaks of hepatitis A. Applied and Environment Microbiology, 75, 7350–7355.

    Article  Google Scholar 

  • Puig, M., Jofre, J., Lucena, F., Allard, A., Wadell, G., & Girones, R. (1994). Detection of adenoviruses and enteroviruses in polluted waters by nested PCR amplification. Applied and Environment Microbiology, 60, 2963–2970.

    CAS  Google Scholar 

  • Pusch, D., Oh, D. Y., Wolf, S., Dumke, R., Schröter-Bobsin, U., Höhne, M., et al. (2005). Detection of enteric viruses and bacterial indicators in German environmental waters. Archives of Virology, 150, 929–947.

    Article  CAS  PubMed  Google Scholar 

  • Ramani, S., & Kang, G. (2009). Viruses causing childhood diarrhea in the developing world. Current Opinion in Infectious Diseases, 22, 477–482.

    Article  PubMed  Google Scholar 

  • Rose, J. B., Singh, S. N., Gerba, C. P., & Kelley, L. M. (1984). Comparison of microporous filters for concentration of viruses from wastewater. Applied and Environment Microbiology, 47, 989–992.

    CAS  Google Scholar 

  • Rzeżutka, A., & Cook, N. (2004). Survival of human enteric viruses in the environment and food. FEMS Microbiology Reviews, 28, 441–453.

    Article  PubMed  Google Scholar 

  • Skraber, S., Gassilloud, B., & Gantzer, C. (2004a). Comparison of coliforms and coliphages as tools for assessment of viral contamination in river water. Applied and Environment Microbiology, 70, 3644–3649.

    Article  CAS  Google Scholar 

  • Skraber, S., Gassilloud, B., Schwartzbrod, L., & Gantzer, C. (2004b). Survival of infectious Poliovirus-1 in river water compared to the persistence of somatic coliphages, thermotolerant coliforms and Poliovirus-1 genome. Water Research, 38, 2927–2933.

    Article  CAS  PubMed  Google Scholar 

  • Smith, E. M., & Gerba, C. P. (1982). Development of a method for detection of human rotavirus in water and sewage. Applied and Environment Microbiology, 43, 1440–1450.

    CAS  Google Scholar 

  • Svraka, S., Duizer, E., Vennema, H., de Bruin, E., van der Veer, B., Dorresteijn, B., et al. (2007). Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005. Journal of Clinical Microbiology, 45(5), 1389–1394.

    Article  PubMed  PubMed Central  Google Scholar 

  • Templeton, M. R., Andrews, R. C., & Hofmann, R. (2008). Particle-associated viruses in water: impacts on disinfection processes. Critical Reviews in Environment Science and Technology, 38, 137–164.

    Article  CAS  Google Scholar 

  • Thompson, S. S., Jackson, J. L., Suva-Castillo, M., Yanko, W. A., El Jack, Z., Kuo, J., et al. (2003). Detection of infectious human adenoviruses in tertiary-treated and ultraviolet-disinfected wastewater. Water Environment Research, 75, 163–170.

    Article  CAS  PubMed  Google Scholar 

  • Van den Berg, H., Lodder, W., van der Poel, W. H. M., Vennema, H., & de Roda Husman, A. M. (2005). Genetic diversity of noroviruses in raw and treated sewage water. Research in Microbiology, 156, 532–540.

    Article  PubMed  Google Scholar 

  • Van Heerden, J., Ehlers, M. M., Van Zyl, W. B., & Grabow, W. O. K. (2003). Incidence of adenoviruses in raw and treated water. Water Research, 37, 3704–3708.

    Article  PubMed  Google Scholar 

  • Vantarakis, A., & Papapetropoulou, M. (1999). Detection of enteroviruses, adenoviruses and hepatitis A viruses in raw sewage and treated effluents by nested-PCR. Water, Air, and Soil pollution, 114, 85–93.

    Article  CAS  Google Scholar 

  • WHO. (1989). Health guidelines for the use of wastewater in agriculture and aquaculture (pp. 74). Report of a WHO Scientific Group. WHO Technical Report Series 778. World Health Organization, Geneva.

  • Wong, K., Mukherjee, B., Kahler, A. M., Zepp, R., & Molina, M. (2012). Influence of inorganic ions on aggregation and adsorption behaviors of human adenovirus. Environmental Science and Technology, 46, 11145–11153.

    Article  CAS  PubMed  Google Scholar 

  • Xagoraraki, I., Yin, Z., & Svambayev, Z. (2014). Fate of viruses in water systems. Journal of Environmental Engineering, 140, 1–18.

    Article  Google Scholar 

  • Weiland, P. & Wulfert, K. (1988). Anaerobic treatment of stillage using different pilot scale fixed bed reactors in up and down mode of operation. In: Proceedings of the 5th International Symposium on Anaerobic Digestion, Bologna, Italy, 147–154.

  • Zhang, T., Breitbart, M., Lee, W. H., Run, J. Q., Wei, C. L., Soh, S. W. L., et al. (2006). RNA viral community in human feces: Prevalence of plant pathogenic viruses. PLoS Biology, 4, 108–118.

    Article  CAS  Google Scholar 

  • Zhang, C. M., Xu, L. M., Xu, P. C., & Wang, X. C. (2016). Elimination of viruses from domestic wastewater: Requirements and technologies. World Journal of Microbiology & Biotechnology, 32, 69–77.

    Article  Google Scholar 

Download references

Acknowledgement

The authors would like to thank the Egyptian Academy of Scientific Research and Technology (ASRT), the Science and Technology Development fund (STDF) for basic, and research Grant No. 1088.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Waled Morsy El-Senousy.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 163 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El-Senousy, W.M., Abou-Elela, S.I. Assessment and Evaluation of an Integrated Hybrid Anaerobic–Aerobic Sewage Treatment System for the Removal of Enteric Viruses. Food Environ Virol 9, 287–303 (2017). https://doi.org/10.1007/s12560-017-9286-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12560-017-9286-4

Keywords

Navigation