Environmental Science and Pollution Research

, Volume 26, Issue 30, pp 30575–30583 | Cite as

Impacts of biofouling on the removal of pharmaceutically active compounds by a nanofiltration membrane

  • Yu YangEmail author
  • Chen Li
  • Li-an Hou
Water Environment Protection and Contamination Treatment


The impacts of biofouling on the retention of pharmaceutically active compounds (PhACs) by a commercially available nanofiltration membrane (NF 270) were systematically studied. Biofouling was achieved through inoculating live and dead Pseudomonas aeruginosa into artificial wastewater. In comparison to a clean membrane, an increase in PhAC rejection during biofouling with live cells was observed. However, the rejection behaviors presented more complex changes during biofouling with dead cells: PhAC rejection was below the clean membrane in the early biofouling stage; however, in the later stage, PhAC rejection was above the clean membrane. In addition, PhAC rejection behaviors present the similar tendency as salt rejection under both biofouling conditions. In addition, solute rejections were much lower for biofouling with dead cells than those for biofouling with live cells. Combined with biofilm characterization under both biofouling conditions, we could conclude that biofilm enhanced osmotic pressure (BEOP) due to higher cell counts and biofilm thickness led to a decrease in PhAC retention, especially for the dead cells. In addition, more dominant steric exclusion in the later stage of biofouling due to higher extracellular polymeric substances (EPS) concentration on the membrane surface resulted in an increase in PhAC retention.


Nanofiltration membrane Pharmaceutically active compounds Biofouling Live cells Dead cells 


Funding information

This study was financially supported by the National Natural Science Foundation of China (Grant No. 51708032 and 51238006).


  1. Azami H, Sarrafzadeh MH, Mehrnia MR (2011) Fouling in membrane bioreactors with various concentrations of dead cells. Desalination 278(1-3):373–380. CrossRefGoogle Scholar
  2. Baker JS, Dudley LY (1998) Biofouling in membrane systems—a review. Desalination 118(1-3):81–90. CrossRefGoogle Scholar
  3. Bayles KW (2007) The biological role of death and lysis in biofilm development. Nat Rev Microbiol 5(9):721–726. CrossRefGoogle Scholar
  4. Bellona C, Drewes JE, Xu P, Amy G (2004) Factors affecting the rejection of organic solutes during NF/RO treatment—a literature review. Water Res 38(12):2795–2809. CrossRefGoogle Scholar
  5. Botton S, Verliefde AR, Quach NT, Cornelissen ER (2012) Influence of biofouling on pharmaceuticals rejection in NF membrane filtration. Water Res 46(18):5848–5860. CrossRefGoogle Scholar
  6. Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. AnBio 72:248–254. CrossRefGoogle Scholar
  7. Bu Q, Wang B, Huang J, Deng S, Yu G (2013) Pharmaceuticals and personal care products in the aquatic environment in China: a review. J Hazard Mater 262:189–211. CrossRefGoogle Scholar
  8. Chang EE, Chang YC, Liang CH, Huang CP, Chiang PC (2012) Identifying the rejection mechanism for nanofiltration membranes fouled by humic acid and calcium ions exemplified by acetaminophen, sulfamethoxazole, and triclosan. J Hazard Mater 221-222:19–27. CrossRefGoogle Scholar
  9. Chen W, Westerhoff P, Leenheer JA, Booksh K (2003) Fluorescence excitation-emission matrix regional integration to quantify spectra for dissolved organic matter. Environ Sci Technol 37(24):5701–5710. CrossRefGoogle Scholar
  10. Chen X, Suwarno SR, Chong TH, McDougald D, Kjelleberg S, Cohen Y, Fane AG, Rice SA (2013) Dynamics of biofilm formation under different nutrient levels and the effect on biofouling of a reverse osmosis membrane system. Biofouling 29(3):319–330. CrossRefGoogle Scholar
  11. Coday BD, Yaffe BG, Xu P, Cath TY (2014) Rejection of trace organic compounds by forward osmosis membranes: a literature review. Environ Sci Technol 48(7):3612–3624. CrossRefGoogle Scholar
  12. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. AnaCh 28(3):350–356. CrossRefGoogle Scholar
  13. Farias EL, Howe KJ, Thomson BM (2014) Spatial and temporal evolution of organic foulant layers on reverse osmosis membranes in wastewater reuse applications. Water Res 58:102–110. CrossRefGoogle Scholar
  14. Habimana O, Semiao AJ, Casey E (2014) Upon impact: the fate of adhering Pseudomonas fluorescens cells during nanofiltration. Environ Sci Technol 48(16):9641–9650. CrossRefGoogle Scholar
  15. Herzberg M, Berry D, Raskin L (2010) Impact of microfiltration treatment of secondary wastewater effluent on biofouling of reverse osmosis membranes. Water Res 44(1):167–176. CrossRefGoogle Scholar
  16. Herzberg M, Elimelech M (2007) Biofouling of reverse osmosis membranes: role of biofilm-enhanced osmotic pressure. J Membr Sci 295(1-2):11–20. CrossRefGoogle Scholar
  17. Herzberg M, Elimelech M (2008) Physiology and genetic traits of reverse osmosis membrane biofilms: a case study with Pseudomonas aeruginosa. ISME J 2(2):180–194. CrossRefGoogle Scholar
  18. Jeong S, Kim S-J, Hee Kim L, Seop Shin M, Vigneswaran S, Vinh Nguyen T, Kim IS (2013) Foulant analysis of a reverse osmosis membrane used pretreated seawater. J Membr Sci 428:434–444. CrossRefGoogle Scholar
  19. Khan MMT, Stewart PS, Moll DJ, Mickols WE, Nelson SE, Camper AK (2011) Characterization and effect of biofouling on polyamide reverse osmosis and nanofiltration membrane surfaces. Biofouling 27(2):173–183. CrossRefGoogle Scholar
  20. Kim LH, Shin MS, Kim S-J, Kim C-M, Chae K-J, Kim IS (2015) Potential effects of damaged Pseudomonas aeruginosa PAO1 cells on development of reverse osmosis membrane biofouling. J Membr Sci 477:86–92. CrossRefGoogle Scholar
  21. Li C, Yang Y, Ding S, Hou L-A (2016) Dynamics of biofouling development on the conditioned membrane and its relationship with membrane performance. J Membr Sci 514:264–273. CrossRefGoogle Scholar
  22. Mahlangu TO, Hoek EMV, Mamba BB, Verliefde ARD (2014) Influence of organic, colloidal and combined fouling on NF rejection of NaCl and carbamazepine: role of solute–foulant–membrane interactions and cake-enhanced concentration polarisation. J Membr Sci 471:35–46. CrossRefGoogle Scholar
  23. Matin A, Khan Z, Zaidi SMJ, Boyce MC (2011) Biofouling in reverse osmosis membranes for seawater desalination: phenomena and prevention. Desalination 281:1–16. CrossRefGoogle Scholar
  24. Nghiem LD, Schafer AI, Elimelech M (2005) Pharmaceutical retention mechanisms by nanofiltration membranes. Environ Sci Technol 39(19):7698–7705. CrossRefGoogle Scholar
  25. Radjenovic J, Petrovic M, Ventura F, Barcelo D (2008) Rejection of pharmaceuticals in nanofiltration and reverse osmosis membrane drinking water treatment. Water Res 42(14):3601–3610. CrossRefGoogle Scholar
  26. Sui Q, Huang J, Deng S, Yu G, Fan Q (2010) Occurrence and removal of pharmaceuticals, caffeine and DEET in wastewater treatment plants of Beijing, China. Water Res 44(2):417–426. CrossRefGoogle Scholar
  27. Valladares Linares R, Yangali-Quintanilla V, Li Z, Amy G (2011) Rejection of micropollutants by clean and fouled forward osmosis membrane. Water Res 45(20):6737–6744. CrossRefGoogle Scholar
  28. Vogel D, Simon A, Alturki AA, Bilitewski B, Price WE, Nghiem LD (2010) Effects of fouling and scaling on the retention of trace organic contaminants by a nanofiltration membrane: the role of cake-enhanced concentration polarisation. Sep Purif Technol 73(2):256–263. CrossRefGoogle Scholar
  29. Wang X-m, Li B, Zhang T, Li X-y (2015) Performance of nanofiltration membrane in rejecting trace organic compounds: experiment and model prediction. Desalination 370:7–16. CrossRefGoogle Scholar
  30. Xue S, Liang L, Zhao Q, Wei L, Ma X, Hou W (2010) Fluorescence characteristics of dissolved organic matter in secondary treated effluents. Environ Sci Technol 33:177–182Google Scholar
  31. Zhang Y, Zhang H, Chu H, Zhou X, Zhao Y (2013) Characterization of dissolved organic matter in a dynamic membrane bioreactor for wastewater treatment. ChSBu 58(15):1717–1724. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.State Key Laboratory of Water Environment Simulation, School of EnvironmentBeijing Normal UniversityBeijingChina
  2. 2.Key Laboratory for Water and Sediment Science of Ministry of Education, School of EnvironmentBeijing Normal UniversityBeijingChina
  3. 3.Xi’ an High-Tech InstituteXi’ anChina

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