How Fiber Breakage Reduces Microorganism Removal in Ultrafiltration for Wastewater Reclamation

  • Suntae LeeEmail author
  • Naoyuki Yamashita
  • Hiroaki Tanaka
Original Paper


Ultrafiltration (UF) membranes are increasingly being used for wastewater reclamation treatment for their high removal of pathogens and suspended solids. However, breakage of UF membrane fibers could allow leakage of pathogens into the permeate and create health risks in the use of reclaimed water. Here, we assessed the log10 reduction value (LRV) of human enteric viruses and microbial indicators of new and aged UF modules in a pilot-scale UF process to evaluate the influence of fiber breakage. Norovirus genotypes I and II, Aichi virus, and Escherichia coli were not detected in any permeate samples of intact UF modules, but were detected in samples of damaged UF modules. LRVs of all microorganisms assayed decreased as fiber breakage of new UF modules increased, with maximum decreases of > 3.3 log10. Fiber breakage in the aged UF modules did not decrease LRVs of somatic coliphages and MS2, but breakage in the new UF modules did decrease them. Intact new UF modules gave higher LRVs than intact aged UF modules. When the LRV of intact UF module was assumed to be 1 or 2 log10, increasing fiber breakage did not significantly decrease the predicted LRV, but when it was ≥ 3 log10, it did decrease LRV, in good agreement with measured LRVs in the degraded UF modules. These results suggest that the LRV of intact UF modules affects the decrease in LRV and confirm the leakage of human enteric viruses following fiber breakage in UF modules of different ages in the UF process of wastewater reclamation.


Ultrafiltration Integrity Microorganism removal Fiber breakage Wastewater reclamation 



This work was supported by a JSPS KAKENHI Grant (15H02273) from the Japan Society for the Promotion of Science (JSPS) and by the Breakthrough by Dynamic Approach in Sewage High Technology (B-DASH) project of the National Institute for Land and Infrastructure Management (NILIM), Japan. The assistance of Yoshiki Sawazaki is highly appreciated. We also thank Seiya Hanamoto for his valuable comments and suggestions.

Supplementary material

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Supplementary material 1 (DOCX 96 KB)


  1. Antony, A., Blackbeard, J., Angles, M., & Leslie, G. (2014). Non-microbial indicators for monitoring virus removal by ultrafiltration membranes. Journal of Membrane Science, 454, 193–199. Scholar
  2. Antony, A., Blackbeard, J., & Leslie, G. (2012). Technology removal efficiency and integrity monitoring techniques for virus removal by membrane processes. Critical Reviews in Environmental Science and Technology, 42, 891–933. Scholar
  3. Asami, T., Katayama, H., Torrey, J. R., Visvanathan, C., & Furumai, H. (2016). Evaluation of virus removal efficiency of coagulation-sedimentation and rapid sand filtration processes in a drinking water treatment plant in Bangkok, Thailand. Water Research, 101, 84–94. Scholar
  4. Boudaud, N., Machinal, C., David, F., Fréval-Le Bourdonnec, A., Jossent, J., Bakanga, F., et al. (2012). Removal of MS2, Qβ and GA bacteriophages during drinking water treatment at pilot scale. Water Research, 46, 2651–2664. Scholar
  5. Brehant, A., Glucina, K., Le Moigne, I., & Laine, J.-M. (2010). Risk management approach for monitoring UF membrane integrity and experimental validation using Ms2-phages. Desalination, 250, 956–960. Scholar
  6. Burutarán, L., Lizasoain, A., García, M., Tort, L. F. L., Colina, R., & Victoria, M. (2016). Detection and molecular characterization of Aichivirus 1 in wastewater samples from Uruguay. Food and Environmental Virology, 8, 13–17. Scholar
  7. Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., et al. (2009). The MIQE guidelines: Minimum information for publication of quanti- tative real-time PCR experiments. Clinical Chemistry, 55, 611–622.CrossRefGoogle Scholar
  8. Elhadidy, A. M., Peldszus, S., & Van Dyke, M. I. (2013). An evaluation of virus removal mechanisms by ultrafiltration membranes using MS2 and phiX174 bacteriophage. Separation and Purification Technology, 120, 215–223. Scholar
  9. Elhadidy, A. M., Peldszus, S., & Van Dyke, M. I. (2014). Effect of hydraulically reversible and hydraulically irreversible fouling on the removal of MS2 and phiX174 bacteriophage by an ultrafiltration membrane. Water Research, 61, 297–307. Scholar
  10. Ferrer, O., Casas, S., Galvañ, C., Lucena, F., Bosch, A., Galofré, B., et al. (2015). Direct ultrafiltration performance and membrane integrity monitoring by microbiological analysis. Water Research, 83, 121–131. Scholar
  11. Furiga, A., Pierre, G., Glories, M., Aimar, P., Roques, C., Causserand, C., et al. (2011). Effects of ionic strength on bacteriophage MS2 behavior and their implications for the assessment of virus retention by ultrafiltration membranes. Applied and Environmental Microbiology, 77, 229–236. Scholar
  12. 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. Scholar
  13. Gijsbertsen-Abrahamse, A. J., Cornelissen, E. R., & Hofman, J. A. M. H. (2006). Fiber failure frequency and causes of hollow fiber integrity loss. Desalination, 194, 251–258. Scholar
  14. Guo, H., Wyart, Y., Perot, J., Nauleau, F., & Moulin, P. (2010). Low-pressure membrane integrity tests for drinking water treatment: A review. Water Research, 44, 41–57. Scholar
  15. Hamza, I. A., Jurzik, L., Überla, 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. Scholar
  16. Haramoto, E., Kitajima, M., Kishida, N., Konno, Y., Katayama, H., Asami, M., et al. (2013). Occurrence of pepper mild mottle virus in drinking water sources in Japan. Applied and Environmental Microbiology, 79, 7413–7418. Scholar
  17. Hirani, Z. M., Bukhari, Z., Oppenheimer, J., Jjemba, P., Lechevallier, M. W., & Jacangelo, J. G. (2014). Impact of MBR cleaning and breaching on passage of selected microorganisms and subsequent inactivation by free chlorine. Water Research, 57, 313–324. Scholar
  18. Huang, H., Young, T. A., Schwab, K. J., & Jacangelo, J. G. (2012). Mechanisms of virus removal from secondary wastewater effluent by low pressure membrane filtration. Journal of Membrane Science, 409–410, 1–8. Scholar
  19. Jacangelo, J. G., Adham, S. S., & Laine, J. M. (1995). Mechanism of cryptosporidium, giardia, and MS2 virus removal by MF and UF. Journal–American Water Works Association, 87, 107–121.CrossRefGoogle Scholar
  20. Jacangelo, J. G., Trussell, R. R., & Watson, M. (1997). Role of membrane technology in drinking water treatment in the United States. Desalination, 113, 119–127. Scholar
  21. 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. Scholar
  22. 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, 488–489, 290–296. Scholar
  23. Kitajima, M., Oka, T., Takagi, H., Tohya, Y., Katayama, H., Takeda, N., et al. (2010). Development and application of a broadly reactive real-time reverse transcription-PCR assay for detection of murine noroviruses. Journal of Virological Methods, 169(2), 269–273. Scholar
  24. Kuroda, K., Nakada, N., Hanamoto, S., Inaba, M., Katayama, H., Do, A. T., et al. (2015). Pepper mild mottle virus as an indicator and a tracer of fecal pollution in water environments: Comparative evaluation with wastewater-tracer pharmaceuticals in Hanoi, Vietnam. Science of the Total Environment, 506–507, 287–298.
  25. Langlet, J., Ogorzaly, L., Schrotter, J. C., Machinal, C., Gaboriaud, F., Duval, J. F. L., et al. (2009). Efficiency of MS2 phage and Qβ phage removal by membrane filtration in water treatment: Applicability of real-time RT-PCR method. Journal of Membrane Science, 326, 111–116. Scholar
  26. Lee, S., Hata, A., Yamashita, N., & Tanaka, H. (2017a). Evaluation of virus reduction by ultrafiltration with coagulation—sedimentation in water reclamation. Food and Environmental Virology, 9, 453–463. Scholar
  27. Lee, S., Ihara, M., Yamashita, N., & Tanaka, H. (2017b). Improvement of virus removal by pilot-scale coagulation-ultrafiltration process for wastewater reclamation: Effect of optimization of pH in secondary effluent. Water Research, 114, 23–30. Scholar
  28. Lee, S., Tasaki, S., Hata, A., Yamashita, N., & Tanaka, H. (2018). Evaluation of virus reduction at a large-scale wastewater reclamation plant by detection of indigenous F-specific RNA bacteriophage genotypes. Environmental Technology. in press. Scholar
  29. Lodder, W. J., Rutjes, S. A., Takumi, K., & de Roda Husman, A. M. (2013). Aichi virus in sewage and surface water, the Netherlands. Emerging Infectious Diseases, 19, 1222–1230. Scholar
  30. Pérez-Sautu, U., Sano, D., Guix, S., Kasimir, G., Pintó, R. M., & Bosch, A. (2012). Human norovirus occurrence and diversity in the Llobregat river catchment, Spain. Environmental Microbiology, 14, 494–502. Scholar
  31. 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. Scholar
  32. Rachmadi, A. T., Kitajima, M., Pepper, I. L., & Gerba, C. P. (2016). Enteric and indicator virus removal by surface flow wetlands. Science of the Total Environment, 542.
  33. Reeve, P., Regel, R., Dreyfus, J., Monis, P., Lau, M., King, B., et al. (2016). Virus removal of new and aged UF membranes at full-scale in a wastewater reclamation plant. Environmental Science: Water Research & Technology, 2, 1014–1021. Scholar
  34. Rosario, K., Symonds, E. M., Sinigalliano, C., Stewart, J., & Breitbart, M. (2009). Pepper mild mottle virus as an indicator of fecal pollution. Applied and Environmental Microbiology, 75, 7261–7267. Scholar
  35. Sano, D., Amarasiri, M., Hata, A., Watanabe, T., & Katayama, H. (2016). Risk management of viral infectious diseases in wastewater reclamation and reuse: Review. Environment International, 91, 220–229. Scholar
  36. 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 & Technology, 50, 9524–9532. Scholar
  37. Sdiri-Loulizi, K., Hassine, M., Aouni, Z., Gharbi-Khelifi, H., Sakly, N., Chouchane, S., et al. (2010). First molecular detection of Aichi virus in sewage and shellfish samples in the Monastir region of Tunisia. Archives of Virology, 155, 1509–1513. Scholar
  38. Shirasaki, N., Matsushita, T., Matsui, Y., & Murai, K. (2017). Assessment of the efficacy of membrane filtration processes to remove human enteric viruses and the suitability of bacteriophages and a plant virus as surrogates for those viruses. Water Research, 115, 29–39. Scholar
  39. Shirasaki, N., Matsushita, T., Matsui, Y., & Yamashita, R. (2018). Evaluation of the suitability of a plant virus, pepper mild mottle virus, as a surrogate of human enteric viruses for assessment of the efficacy of coagulation-rapid sand filtration to remove those viruses. Water Research, 129, 460–469. Scholar
  40. Van Voorthuizen, E. M., Ashbolt, N. J., & Schäfer, A. I. (2001). Role of hydrophobic and electrostatic interactions for initial enteric virus retention by MF membranes. Journal of Membrane Science, 194, 69–79. Scholar
  41. Yasui, N., Suwa, M., Sakurai, K., Suzuki, Y., Tsumori, J., Kobayashi, K., et al. (2016). Removal characteristics and fluctuation of norovirus in a pilot-plant by an ultrafiltration membrane for the reclamation of treated sewage. Environmental Technology, 3330, 1–9. Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Research Center for Environmental Quality Management, Graduate School of EngineeringKyoto UniversityOtsuJapan
  2. 2.Innovative Materials and Resources Research CenterPublic Works Research InstituteTsukubaJapan

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