State-of-the-Art Reviews
Apr 25, 2020

Removal of Viruses in Membrane Bioreactors

Publication: Journal of Environmental Engineering
Volume 146, Issue 7

Abstract

This review seeks to summarize the current literature regarding the removal of viruses from wastewater using membrane bioreactors (MBRs). Membrane bioreactors are an effective technology for the removal of viruses from wastewater and do so with greater efficiency than conventional activated sludge treatment plants. However, much is unclear about the capabilities and mechanisms of this process. Membrane pore size is commonly thought to be an important factor impacting virus removal, but this effect is primarily observed when the pore size is smaller than the virus diameter, and the effects vary by virus. A variety of factors can impact the effectiveness of MBRs in virus removal, with the presence of a biofilm foremost among them. Balancing the presence of a biofilm with regular membrane backwashing and cleaning to maintain consistent flux remains a critical consideration in MBR operation. Differences in reported removal efficiencies of human viruses compared to model viruses (such as bacteriophages) call into question the reliability of these model viruses in assessing the effectiveness of virus removal in MBRs. More investigation, particularly with full-scale MBR systems, must be performed to further understand the potential of MBRs in virus removal.

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Data Availability Statement

All data, models, and code generated or used during the study appear in the published article.

References

Aidan, A., M. Mehrvar, T. H. Ibrahim, and V. Nenov. 2007. “Particulates and bacteria removal by ceramic microfiltration, UV photolysis, and their combination.” J. Environ. Sci. Health Part A 42 (7): 895–901. https://doi.org/10.1080/10934520701369941.
Asano, T. 2007. Water reuse: Issues, technologies, and applications. New York: McGraw-Hill.
Branch, A., T. Trinh, G. Carvajal, G. Leslie, H. M. Coleman, R. M. Stuetz, J. E. Drewes, S. J. Khan, and P. Le-Clech. 2016. “Hazardous events in membrane bioreactors. 3: Impacts on microorganism log removal efficiencies.” J. Membr. Sci. 497 (Jan): 514–523. https://doi.org/10.1016/j.memsci.2015.10.011.
Castignolles, N., F. Petit, I. Mendel, L. Simon, L. Cattolico, and C. Buffet-Janvresse. 1998. “Detection of adenovirus in the waters of the seine river estuary by nested-PCR.” Mol. Cell. Probes 12 (3): 175–180. https://doi.org/10.1006/mcpr.1998.0166.
Chaudhry, R. M., R. W. Holloway, T. Y. Cath, and K. L. Nelson. 2015a. “Impact of virus surface characteristics on removal mechanisms within membrane bioreactors.” Water Res. 84 (Nov): 144–152. https://doi.org/10.1016/j.watres.2015.07.020.
Chaudhry, R. M., K. L. Nelson, and J. E. Drewes. 2015b. “Mechanisms of pathogenic virus removal in a full-scale membrane bioreactor.” Environ. Sci. Technol. 49 (5): 2815–2822. https://doi.org/10.1021/es505332n.
Choi, J.-G., T.-H. Bae, J.-H. Kim, T.-M. Tak, and A. A. Randall. 2002. “The behavior of membrane fouling initiation on the crossflow membrane bioreactor system.” J. Membr. Sci. 203 (1): 103–113. https://doi.org/10.1016/S0376-7388(01)00790-6.
Çiçek, N., J. P. Franco, M. T. Suidan, V. Urbain, and J. Manem. 1999. “Characterization and comparison of a membrane bioreactor and a conventional activated-sludge system in the treatment of wastewater containing high-molecular-weight compounds.” Water Environ. Res. 71 (1): 64–70. https://doi.org/10.2175/106143099X121481.
Cornel, P., and S. Krause. 2008. “Membrane bioreactors for wastewater treatment.” In Advanced membrane technology and applications, 217–238. New York: Wiley.
da Silva, A. K., J.-C. Le Saux, S. Parnaudeau, M. Pommepuy, M. Elimelech, and F. S. Le Guyader. 2007. “Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: Different behaviors of genogroups I and II.” Appl. Environ. Microbiol. 73 (24): 7891–7897. https://doi.org/10.1128/AEM.01428-07.
De Luca, G., R. Sacchetti, E. Leoni, and F. Zanetti. 2013. “Removal of indicator bacteriophages from municipal wastewater by a full-scale membrane bioreactor and a conventional activated sludge process: Implications to water reuse.” Bioresour. Technol. 129 (Feb): 526–531. https://doi.org/10.1016/j.biortech.2012.11.113.
Fiksdal, L., and T. Leiknes. 2006. “The effect of coagulation with MF/UF membrane filtration for the removal of virus in drinking water.” J. Membr. Sci. 279 (1): 364–371. https://doi.org/10.1016/j.memsci.2005.12.023.
Fox, R., and D. Stuckey. 2015. “MS-2 and T4 phage removal in an anaerobic membrane bioreactor (AnMBR): Effect of gas sparging rate.” J. Chem. Technol. Biotechnol. 90 (3): 384–390. https://doi.org/10.1002/jctb.4586.
Francy, D. S., E. A. Stelzer, R. N. Bushon, A. M. G. Brady, A. G. Williston, K. R. Riddell, M. A. Borchardt, S. K. Spencer, and T. M. Gellner. 2012. “Comparative effectiveness of membrane bioreactors, conventional secondary treatment, and chlorine and UV disinfection to remove microorganisms from municipal wastewaters.” Water Res. 46 (13): 4164–4178. https://doi.org/10.1016/j.watres.2012.04.044.
Gallas-Lindemann, C., I. Sotiriadou, J. Plutzer, and P. Karanis. 2013. “Prevalence and distribution of Cryptosporidium and Giardia in wastewater and the surface, drinking and ground waters in the Lower Rhine, Germany.” Epidemiol. Infect. 141 (1): 9–21. https://doi.org/10.1017/S0950268812002026.
Gao, M., M. Yang, H. Li, Q. Yang, and Y. Zhang. 2004. “Comparison between a submerged membrane bioreactor and a conventional activated sludge system on treating ammonia-bearing inorganic wastewater.” J. Biotechnol. 108 (3): 265–269. https://doi.org/10.1016/j.jbiotec.2003.12.002.
González, S., M. Petrovic, and D. Barceló. 2007. “Removal of a broad range of surfactants from municipal wastewater: Comparison between membrane bioreactor and conventional activated sludge treatment.” Chemosphere 67 (2): 335–343. https://doi.org/10.1016/j.chemosphere.2006.09.056.
Guo, B., E. V. Pasco, I. Xagoraraki, and V. V. Tarabara. 2015. “Virus removal and inactivation in a hybrid microfiltration: UV process with a photocatalytic membrane.” Sep. Purif. Technol. 149 (Jul): 245–254. https://doi.org/10.1016/j.seppur.2015.05.039.
Guo, B., S. D. Snow, B. J. Starr, I. Xagoraraki, and V. V. Tarabara. 2018. “Photocatalytic inactivation of human adenovirus 40: Effect of dissolved organic matter and prefiltration.” Sep. Purif. Technol. 193 (Mar): 193–201. https://doi.org/10.1016/j.seppur.2017.11.012.
Havelaar, A. H., M. van Olphen, and Y. C. Drost. 1993. “F-specific RNA bacteriophages are adequate model organisms for enteric viruses in fresh water.” Appl. Environ. Microbiol. 59 (9): 2956–2962. https://doi.org/10.1128/AEM.59.9.2956-2962.1993.
Herrera-Robledo, M., J. M. Morgan-Sagastume, and A. Noyola. 2010. “Biofouling and pollutant removal during long-term operation of an anaerobic membrane bioreactor treating municipal wastewater.” Biofouling 26 (1): 23–30. https://doi.org/10.1080/08927010903243923.
Hirani, Z. M., J. F. DeCarolis, S. S. Adham, and J. G. Jacangelo. 2010. “Peak flux performance and microbial removal by selected membrane bioreactor systems.” Water Res. 44 (8): 2431–2440. https://doi.org/10.1016/j.watres.2010.01.003.
Holbrook, R. D., K. A. Massie, and J. T. Novak. 2005. “A comparison of membrane bioreactor and conventional-activated-sludge mixed liquor and biosolids characteristics.” Water Environ. Res. 77 (4): 323–330. https://doi.org/10.1002/j.1554-7531.2005.tb00291.x.
Huang, X., Z. Zhao, D. Hernandez, and S. C. Jiang. 2016. “Near real-time flow cytometry monitoring of bacterial and viral removal efficiencies during water reclamation processes.” Water 8 (10): 464. https://doi.org/10.3390/w8100464.
Jumat, M. R., N. A. Hasan, P. Subramanian, C. Heberling, R. R. Colwell, and P.-Y. Hong. 2017. “Membrane bioreactor-based wastewater treatment plant in Saudi Arabia: Reduction of viral diversity, load, and infectious capacity.” Water 9 (7): 534. https://doi.org/10.3390/w9070534.
Kuo, D. H.-W., F. J. Simmons, S. Blair, E. Hart, J. B. Rose, and I. Xagoraraki. 2010. “Assessment of human adenovirus removal in a full-scale membrane bioreactor treating municipal wastewater.” Water Res. 44 (5): 1520–1530. https://doi.org/10.1016/j.watres.2009.10.039.
Leclerc, H., S. Edberg, V. Pierzo, and J. M. Delattre. 2000. “Bacteriophages as indicators of enteric viruses and public health risk in groundwaters.” J. Appl. Microbiol. 88 (1): 5–21. https://doi.org/10.1046/j.1365-2672.2000.00949.x.
Li, H., M. Yang, Y. Zhang, X. Liu, M. Gao, and Y. Kamagata. 2005. “Comparison of nitrification performance and microbial community between submerged membrane bioreactor and conventional activated sludge system.” Water Sci. Technol. 51 (6–7): 193–200. https://doi.org/10.2166/wst.2005.0638.
Liu, R., X. Huang, R. Liu, and Y. Qian. 2001. “A comparison between a submerged membrane bioreactor and a conventional activated sludge process.” Chin. J. Environ. Sci. 22 (3): 20–24.
Lu, R., Q. Li, Z. Yin, I. Xagoraraki, V. V. Tarabara, and T. H. Nguyen. 2016. “Effect of virus influent concentration on its removal by microfiltration: The case of human adenovirus 2.” J. Membr. Sci. 497 (Jan): 120–127. https://doi.org/10.1016/j.memsci.2015.08.065.
Lv, W., X. Zheng, M. Yang, Y. Zhang, Y. Liu, and J. Liu. 2006. “Virus removal performance and mechanism of a submerged membrane bioreactor.” Process Biochem. 41 (2): 299–304. https://doi.org/10.1016/j.procbio.2005.06.005.
Madigan, M. T., and J. M. Martinko. 2006. “Microorganisms and microbiology.” In Brock biology of microorganisms. 11th ed. 1–20. Upper Saddle River, NJ: Pearson Prentice Hall.
Melnick, J. L., C. P. Gerba, and C. Wallis. 1978. “Viruses in water.” Bull. World Health Organ. 56 (4): 499–508.
Miura, T., S. Okabe, Y. Nakahara, and D. Sano. 2015. “Removal properties of human enteric viruses in a pilot-scale membrane bioreactor (MBR) process.” Water Res. 75 (May): 282–291. https://doi.org/10.1016/j.watres.2015.02.046.
Miura, T., J. Schaeffer, J.-C. Le Saux, P. Le Mehaute, and F. S. Le Guyader. 2018. “Virus type-specific removal in a full-scale membrane bioreactor treatment process.” Food Environ. Virol. 10 (2): 176–186. https://doi.org/10.1007/s12560-017-9330-4.
Munz, G., M. Gualtiero, L. Salvadori, B. Claudia, and L. Claudio. 2008. “Process efficiency and microbial monitoring in MBR (membrane bioreactor) and CASP (conventional activated sludge process) treatment of tannery wastewater.” Bioresour. Technol. 99 (18): 8559–8564. https://doi.org/10.1016/j.biortech.2008.04.006.
O’Brien, E., M. Munir, T. Marsh, M. Heran, G. Lesage, V. V. Tarabara, and I. Xagoraraki. 2017a. “Diversity of DNA viruses in effluents of membrane bioreactors in Traverse City, MI (USA) and La Grande Motte (France).” Water Res. 111 (Mar): 338–345. https://doi.org/10.1016/j.watres.2017.01.014.
O’Brien, E., J. Nakyazze, H. Wu, N. Kiwanuka, W. Cunningham, J. B. Kaneene, and I. Xagoraraki. 2017b. “Viral diversity and abundance in polluted waters in Kampala, Uganda.” Water Res. 127 (Dec): 41–49. https://doi.org/10.1016/j.watres.2017.09.063.
Ottoson, J., A. Hansen, B. Björlenius, H. Norder, and T. A. Stenström. 2006. “Removal of viruses, parasitic protozoa and microbial indicators in conventional and membrane processes in a wastewater pilot plant.” Water Res. 40 (7): 1449–1457. https://doi.org/10.1016/j.watres.2006.01.039.
Prado, T., A. de Castro Bruni, M. R. F. Barbosa, S. C. Garcia, L. Z. Moreno, and M. I. Z. Sato. 2019. “Noroviruses in raw sewage, secondary effluents and reclaimed water produced by sand-anthracite filters and membrane bioreactor/reverse osmosis system.” Sci. Total Environ. 646 (Jan): 427–437. https://doi.org/10.1016/j.scitotenv.2018.07.301.
Puig, M., J. Jofre, F. Lucena, A. Allard, G. Wadell, and R. Girones. 1994. “Detection of adenoviruses and enteroviruses in polluted waters by nested PCR amplification.” Appl. Environ. Microbiol. 60 (8): 2963–2970. https://doi.org/10.1128/AEM.60.8.2963-2970.1994.
Purnell, S., J. Ebdon, A. Buck, M. Tupper, and H. Taylor. 2015. “Bacteriophage removal in a full-scale membrane bioreactor (MBR): Implications for wastewater reuse.” Water Res. 73 (Apr): 109–117. https://doi.org/10.1016/j.watres.2015.01.019.
Saddoud, A., M. Ellouze, A. Dhouib, and S. Sayadi. 2007. “Anaerobic membrane bioreactor treatment of domestic wastewater in Tunisia.” Desalination 207 (1): 205–215. https://doi.org/10.1016/j.desal.2006.08.005.
Shang, C., H. M. Wong, and G. Chen. 2005. “Bacteriophage MS-2 removal by submerged membrane bioreactor.” Water Res. 39 (17): 4211–4219. https://doi.org/10.1016/j.watres.2005.08.003.
Silva, C. C., E. C. Jesus, A. P. R. Torres, M. P. Sousa, V. M. J. Santiago, and V. M. Oliveira. 2010. “Investigation of bacterial diversity in membrane bioreactor and conventional activated sludge processes from petroleum refineries using phylogenetic and statistical approaches.” J. Microbiol. Biotechnol. 20 (3): 447–459. https://doi.org/10.4014/jmb.0906.06052.
Sima, L. C., J. Schaeffer, J.-C. Le Saux, S. Parnaudeau, M. Elimelech, and F. S. Le Guyader. 2011. “Calicivirus removal in a membrane bioreactor wastewater treatment plant.” Appl. Environ. Microbiol. 77 (15): 5170–5177. https://doi.org/10.1128/AEM.00583-11.
Simmons, F. J., D. H.-W. Kuo, and I. Xagoraraki. 2011. “Removal of human enteric viruses by a full-scale membrane bioreactor during municipal wastewater processing.” Water Res. 45 (9): 2739–2750. https://doi.org/10.1016/j.watres.2011.02.001.
Simmons, F. J., and I. Xagoraraki. 2011. “Release of infectious human enteric viruses by full-scale wastewater utilities.” Water Res. 45 (12): 3590–3598. https://doi.org/10.1016/j.watres.2011.04.001.
Soriano, G. A., M. Erb, C. Garel, and J. M. Audic. 2003. “A comparative pilot-scale study of the performance of conventional activated sludge and membrane bioreactors under limiting operating conditions.” Water Environ. Res. 75 (3): 225–231. https://doi.org/10.2175/106143003X141006.
Tam, L. S., T. W. Tang, G. N. Lau, K. R. Sharma, and G. H. Chen. 2007. “A pilot study for wastewater reclamation and reuse with MBR/RO and MF/RO systems.” Desalination 202 (1): 106–113. https://doi.org/10.1016/j.desal.2005.12.045.
USEPA. 2015. Review of coliphages as possible indicators of fecal contamination for ambient water quality. Washington, DC: USEPA.
Wong, K., T.-T. Fong, K. Bibby, and M. Molina. 2012. “Application of enteric viruses for fecal pollution source tracking in environmental waters.” Environ. Int. 45 (Sep): 151–164. https://doi.org/10.1016/j.envint.2012.02.009.
Wu, J., H. Li, and X. Huang. 2010. “Indigenous somatic coliphage removal from a real municipal wastewater by a submerged membrane bioreactor.” Water Res. 44 (6): 1853–1862. https://doi.org/10.1016/j.watres.2009.12.013.
Xagoraraki, I., Z. Yin, and Z. Svambayev. 2014. “Fate of viruses in water systems.” J. Environ. Eng. 140 (7): 04014020. https://doi.org/10.1061/(ASCE)EE.1943-7870.0000827.
Xiao, K., S. Liang, X. Wang, C. Chen, and X. Huang. 2019. “Current state and challenges of full-scale membrane bioreactor applications: A critical review.” Bioresour. Technol. 271 (Jan): 473–481. https://doi.org/10.1016/j.biortech.2018.09.061.
Yin, Z., V. V. Tarabara, and I. Xagoraraki. 2015. “Human adenovirus removal by hollow fiber membranes: Effect of membrane fouling by suspended and dissolved matter.” J. Membr. Sci. 482 (May): 120–127. https://doi.org/10.1016/j.memsci.2015.02.028.
Yin, Z., V. V. Tarabara, and I. Xagoraraki. 2016. “Effect of pressure relaxation and membrane backwash on adenovirus removal in a membrane bioreactor.” Water Res. 88 (Jan): 750–757. https://doi.org/10.1016/j.watres.2015.10.066.
Yin, Z., and I. Xagoraraki. 2014. “Membrane bioreactors (MBRs) for water reuse in the USA.” In Advanced treatment technologies for urban wastewater reuse, edited by D. Fatta-Kassinos, D. D. Dionysiou, and K. Kümmerer, 223–245. Cham, Switzerland: Springer.
Zanetti, F., G. De Luca, and R. Sacchetti. 2010. “Performance of a full-scale membrane bioreactor system in treating municipal wastewater for reuse purposes.” Bioresour. Technol. 101 (10): 3768–3771. https://doi.org/10.1016/j.biortech.2009.12.091.
Zheng, X., and J. Liu. 2007. “Virus rejection with two model human enteric viruses in membrane bioreactor system.” Sci. China, Ser. B Chem. 50 (3): 397–404. https://doi.org/10.1007/s11426-007-0047-3.
Zheng, X., W. Lü, M. Yang, and J. Liu. 2005. “Evaluation of virus removal in MBR using coliphages T4.” Chin. Sci. Bull. 50 (9): 862–867. https://doi.org/10.1360/04wb0087.

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Go to Journal of Environmental Engineering
Journal of Environmental Engineering
Volume 146Issue 7July 2020

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Published online: Apr 25, 2020
Published in print: Jul 1, 2020
Discussion open until: Sep 25, 2020

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Evan O’Brien [email protected]
Graduate Student, Dept. of Civil and Environmental Engineering, Michigan State Univ., A10 Engineering Research Complex, East Lansing, MI 48824 (corresponding author). Email: [email protected]
Irene Xagoraraki, M.ASCE [email protected]
Associate Professor, Dept. of Civil and Environmental Engineering, Michigan State Univ., A124 Engineering Research Complex, East Lansing, MI 48824. Email: [email protected]

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