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Review

Virus filtration in biopharmaceutical downstream processes: key factors and current limitations

, , &
Pages 26-39 | Received 02 Aug 2021, Accepted 25 Oct 2022, Published online: 14 Nov 2022

References

  • Merten, O.-W. Virus Contaminations of Cell Cultures - A Biotechnological View. Cytotechnology. 2002, 39(2), 91–116. DOI: 10.1023/A:1022969101804.
  • Barone, P. W.; Wiebe, M. E.; Leung, J. C.; Hussein, I. T. M.; Keumurian, F. J.; Bouressa, J.; Brussel, A.; Chen, D.; Chong, M.; Dehghani, H., et al. Viral Contamination in Biologic Manufacture and Implications for Emerging Therapies. Nat. Biotechnol. 2020, 38, 563–572. DOI: 10.1038/s41587-020-0507-2.
  • Shukla, A. A.; Aranha, H. Viral Clearance for Biopharmaceutical Downstream Processes. Pharmaceutical Bioprocessing. 2015, 3, 127–138. DOI: 10.4155/pbp.14.62.
  • ICH. International Conference on Harmonisation. Guidance on Viral Safety Evaluation of Biotechnology Products Derived from Cell Lines of Human or Animal Origin Q5A (R1); availability – FDA. Notice. Federal Register. 1998, 63, 51074–57084.
  • EMA. Guideline on Virus Safety Evaluation of Biotechnological Investigational Medicinal Products. EMA Guide. 2008, 1–14.
  • Ajayi, O. O.; Johnson, S. A.; Faison, T.; Azer, N.; Jackie, L.; Dement-brown, J.; Lute, S. C. An Updated Analysis of Viral Clearance Unit Operations for Biotechnology Manufacturing. Current reserach in Biotechnology. 2022. DOI: 10.1016/j.crbiot.2022.03.002.
  • Zydney, A. L. Continuous Downstream Processing for High Value Biological Products: A Review. Biotechnol. Bioeng. 2016, 113, 465–475. DOI: 10.1002/bit.25695.
  • Miesegaes, G.; Lute, S.; Brorson, K. Analysis of Viral Clearance Unit Operations for Monoclonal Antibodies. Biotechnol. Bioeng. 2010, 106, 238–246. DOI: 10.1002/bit.22662.
  • Bakhshayeshi, M.; Zydney, A. L. Effect of Solution PH on Protein Transmission and Membrane Capacity during Virus Filtration. Biotechnol. Bioeng. 2008, 100, 108–117. DOI: 10.1002/bit.21735.
  • PDA. Technical Report No. 41 Virus Filtration. . https://www.pda.org/bookstore/product-detail/6725-tr-41-revised-virus-filtration (accessed 2020).
  • Remington, K. M. Fundamental Strategies for Viral Clearance. Part 2: Technical Approaches . Bioprocess Int., 2015, 13. https://bioprocessintl.com/wp-content/uploads/2015/05/13-5-Remington-Secured1.pdf (accessed12 May 2015).
  • Joshi, P. U.; Meingast, C. L.; Xu, X.; Holstein, M.; Feroz, H.; Ranjan, S.; Ghose, S.; Li, Z. J.; Heldt, C. L. Virus Inactivation at Moderately Low PH Varies with Virus and Buffer Properties. Biotechnol. J. 2021, 2100320. 10.1002/biot.202100320.This.
  • Gefroh, E.; Dehghani, H.; McClure, M.; Connell-Crowley, L.; Vedantham, G. Use of MMV as a Single Worst-Case Model Virus in Viral Filter Validation Studies. Journal of pharmaceutical science technology. 2014, 68, 297–311. DOI: 10.5731/pdajpst.2014.00978.
  • Kern, G.; Krishnan, M . Virus Removal by Filtration: Points to Consider. BioPharm. Int. 19(10) . https://www.biopharminternational.com/view/virus-removal-filtration-points-consider (Accessed 01 October 2020).
  • Dileo, A. J.; Allegrezza, J.; Anthony, E.; Builder, S. E. High Resolution Removal of Virus from Protein Solutions Using a Membrane of Unique Structure. Nat. Biotechnol. 1992, 10, 182–188. DOI: 10.1038/nbt0292-182.
  • Syedain, Z. H.; Bohonak, D. M.; Zydney, A. L. Protein Fouling of Virus Filtration Membranes: Effects of Membrane Orientation and Operating Conditions. Biotechnol. Prog. 2006, 22, 1163–1169. DOI: 10.1021/bp050350v.
  • Lute, S.; Aranha, H.; Tremblay, D.; Liang, D.; Ackermann, H. W.; Chu, B.; Moineau, S.; Brorson, K. Characterization of Coliphage PR772 and Evaluation of Its Use for Virus Filter Performance Testing. Appl. Environ. Microbiol. 2004, 70, 4864–4871. DOI: 10.1128/AEM.70.8.4864-4871.2004.
  • PDA . Phage Retention Nomenclature Rating for Small- and Large- Virus Retentive Filters (Single User Digital Version). PDA standard. 2021. https://www.pda.org/bookstore/product-detail/6038-pda-standard-04-2021 (Accessed 2020).
  • Marques, B. F.; Roush, D. J.; Göklen, K. E. Virus Filtration of High-Concentration Monoclonal Antibody Solutions. Biotechnol. Prog. 2009, 25, 483–491. DOI: 10.1002/btpr.177.
  • Hawe, A.; Kasper, J. C.; Friess, W.; Jiskoot, W. Structural Properties of Monoclonal Antibody Aggregates Induced by Freeze-Thawing and Thermal Stress. Eur. J. Pharm. Sci. 2009, 38, 79–87. DOI: 10.1016/j.ejps.2009.06.001.
  • Brough, H.; Antoniou, C.; Carter, J.; Jakubik, J.; Xu, Y.; Lutz, H. Performance of a Novel Viresolve NFR Virus Filter. Biotechnol. Prog. 2002, 18, 782–795. DOI: 10.1021/bp010193.
  • Sekine, S.; Komuro, M.; Sohka, T.; Sato, T. Integrity Testing of PlanovaTM BioEX Virus Removal Filters Used in the Manufacture of Biological Products. Biologicals. 2015, 43, 186–194. DOI: 10.1016/j.biologicals.2015.02.003.
  • Roberts, P. L.; Feldman, P.; Crombie, D.; Walker, C.; Lowery, K. Virus Removal from Factor IX by Filtration: Validation of the Integrity Test and Effect of Manufacturing Process Conditions. Biologicals. 2010, 38, 303–310. DOI: 10.1016/j.biologicals.2009.12.006.
  • van Reis, R.; Zydney, A. Bioprocess Membrane Technology. J. Memb. Sci. 2007, 297, 16–50. DOI: 10.1016/j.memsci.2007.02.045.
  • Zydney, A. L. New Developments in Membranes for Bioprocessing – A Review. J. Memb. Sci. 2021, 620, 118804. DOI: 10.1016/j.memsci.2020.118804.
  • Burnouf, T.; Radosevich, M. Nanofiltration of Plasma-Derived Biopharmaceutical Products. Haemophilia. 2003, 9, 24–37. DOI: 10.1046/j.1365-2516.2003.00701.x.
  • Ide, S. Filter Made of Cuprammonium Regenerated Cellulose for Virus Removal: A Mini-Review. Cellulose. 2022, 29, 2779–2793. DOI: 10.1007/s10570-021-04319-2.
  • Junter, G. A.; Lebrun, L. Cellulose-Based Virus-Retentive Filters: A Review. Rev. Environ. Sci. Biotechnol. 2017, 16, 455–489. DOI: 10.1007/s11157-017-9434-1.
  • Johnson, S. A.; Chen, S.; Bolton, G.; Chen, Q.; Lute, S.; Fisher, J.; Brorson, K. Virus Filtration: A Review of Current and Future Practices in Bioprocessing. Biotechnol. Bioeng. 2022, 119, 743–761. DOI: 10.1002/bit.28017.
  • Nejatishahidein, N.; Zydney, A. L. Depth Filtration in Bioprocessing — New Opportunities for an Old Technology. Current opinion chemical engineering. 2021, 34, 100746. DOI: 10.1016/j.coche.2021.100746.
  • Wickramasinghe, S. R.; Stump, E. D.; Grzenia, D. L.; Husson, S. M.; Pellegrino, J. Understanding Virus Filtration Membrane Performance. J. Memb. Sci. 2010, 365, 160–169. DOI: 10.1016/j.memsci.2010.09.002.
  • Charcosset, C. Membrane Processes in Biotechnology and Pharmaceutics; United Kingdom: Elsevier, 2012.
  • Kosiol, P.; Müller, M. T.; Schneider, B.; Hansmann, B.; Thom, V.; Ulbricht, M. Determination of Pore Size Gradients of Virus Filtration Membranes Using Gold Nanoparticles and Their Relation to Fouling with Protein Containing Feed Streams. J. Memb. Sci. 2018, 548, 598–608. DOI: 10.1016/j.memsci.2017.11.048.
  • Fallahianbijan, F.; Giglia, S.; Carbrello, C.; Bell, D.; Zydney, A. L. Impact of Protein Fouling on Nanoparticle Capture within the Viresolve® Pro and Viresolve® NFP Virus Removal Membranes. Biotechnol. Bioeng. 2019, 116, 2285–2291. DOI: 10.1002/bit.27017.
  • Fallahianbijan, F.; Giglia, S.; Carbrello, C.; Zydney, A. L. Quantitative Analysis of Internal Flow Distribution and Pore Interconnectivity within Asymmetric Virus Filtration Membranes. J. Memb. Sci. 2020, 595, 117578. DOI: 10.1016/j.memsci.2019.117578.
  • Brickey, K. P.; Zydney, A. L.; Gomez, E. D. FIB-SEM Tomography Reveals the Nanoscale 3D Morphology of Virus Removal Filters. J. Memb. Sci. 2021, 640, 119766. DOI: 10.1016/j.memsci.2021.119766.
  • Bakhshayeshi, M.; Jackson, N.; Kuriyel, R.; Mehta, A.; van Reis, R.; Zydney, A. L. Use of Confocal Scanning Laser Microscopy to Study Virus Retention during Virus Filtration. J. Memb. Sci. 2011, 379, 260–267. DOI: 10.1016/j.memsci.2011.05.069.
  • Nazem-Bokaee, H.; Fallahianbijan, F.; Chen, D.; O’Donnell, S. M.; Carbrello, C.; Giglia, S.; Bell, D.; Zydney, A. L. Probing Pore Structure of Virus Filters Using Scanning Electron Microscopy with Gold Nanoparticles. J. Memb. Sci. 2018, 552, 144–152. DOI: 10.1016/j.memsci.2018.01.069.
  • Van Voorthuizen, E. M.; Ashbolt, N. J.; Schäfer, A. I. Role of Hydrophobic and Electrostatic Interactions for Initial Enteric Virus Retention by MF Membranes. J. Memb. Sci. 2001, 194, 69–79. DOI: 10.1016/S0376-7388(01)00522-1.
  • Gerba, C. P. Applied and Theoretical Aspects of Virus Adsorption to Surfaces. Adv. Appl. Microbiol. 1984, 30, 133–168. DOI: 10.1016/S0065-2164(08)70054-6.
  • Moore, R. S.; Taylor, D. H.; Sturman, L. S.; Reddy, M. M.; Fuhs, G. W. Poliovirus Adsorption by 34 Minerals and Soils. Appl. Environ. Microbiol. 1981, 42, 963–975. DOI: 10.1128/aem.42.6.963-975.1981.
  • Cookson, J. T.; North, W. J. Adsorption of Viruses on Activated Carbon. Equilibriums and Kinetics of the Attachment of Escherichia Coli Bacteriophage T4 on Activated Carbon. Environ. Sci. Technol. 1967, 1, 46–52. DOI: 10.1021/es60001a002.
  • Wang, D.; Gerba, C. P.; Lance, J. C. Effect of Soil Permeability on Virus Removal through Soil Columns. Appl. Environ. Microbiol. 1981, 42, 83–88. DOI: 10.1128/aem.42.1.83-88.1981.
  • Dowd, S. E.; Pillai, S. D.; Wang, S.; Corapcioglu, M. Y. Delineating the Specific Influence of Virus Isoelectric Point and Size on Virus Adsorption and Transport through Sandy Soils. Appl. Environ. Microbiol. 1998, 64, 405–410. DOI: 10.1128/aem.64.2.405-410.1998.
  • Dika, C.; Duval, J. F. L.; Francius, G.; Perrin, A.; Gantzer, C. Isoelectric Point Is an Inadequate Descriptor of MS2, Phi X 174 and PRD1 Phages Adhesion on Abiotic Surfaces. J. Colloid Interface Sci. 2015, 446, 327–334. DOI: 10.1016/j.jcis.2014.08.055.
  • Heffron, J.; Mayer, B. K. Virus Isoelectric Point Estimation: Theories and Methods. Appl. Environ. Microbiol. 2021, 87, 1–17. DOI: 10.1128/AEM.02319-20.
  • LaBelle, R. L.; Gerba, C. P. Influence of PH, Salinity, and Organic Matter on the Adsorption of Enteric Viruses to Estuarine Sediment. Appl. Environ. Microbiol. 1979, 38, 93–101. DOI: 10.1128/aem.38.1.93-101.1979.
  • Stanevich, V.; Pachalla, A.; Nunez, B.; McInnes, M.; Nieder, C.; Schreffler, J. Improving Viral Filtration Capacity in Biomanufacturing Processes Using Aggregate Binding Properties of Polyamide-6,6. Biotechnol. Bioeng. 2021, 118, 1105–1115. DOI: 10.1002/bit.27634.
  • Heldt, C. L.; Zahid, A.; Vijayaragavan, K. S.; Mi, X. Experimental and Computational Surface Hydrophobicity Analysis of a Non-Enveloped Virus and Proteins. Colloids Surf. B Biointerfaces. 2017, 153, 77–84. DOI: 10.1016/j.colsurfb.2017.02.011.
  • Goodrich, E. M.; Bohonak, D. M.; Genest, P. W.; Peterson, E. Chapter 7 - Recent advances in ultrafiltration and virus filtration for production of antibodies and related biotherapeutics Approaches to the Purification, Analysis and Characterization of Antibody-Based Therapeutics. Canada. 2020,137–166. DOI: 10.1016/B978-0-08-103019-6.00007-2.
  • Fröhlich, H.; Villian, L.; Melzner, D.; Strube, J. Membrane Technology in Bioprocess Science. Chemie-Ingenieur-Technik. 2012, 84, 905–917. DOI: 10.1002/cite.201200025.
  • Brown, A.; Bechtel, C.; Bill, J.; Liu, H.; Liu, J.; McDonald, D.; Pai, S.; Radhamohan, A.; Renslow, R.; Thayer, B., et al. Increasing Parvovirus Filter Throughput of Monoclonal Antibodies Using Ion Exchange Membrane Adsorptive Pre-Filtration. Biotechnol. Bioeng. 2010, 106, 627–637. DOI: 10.1002/bit.22729.
  • AsahiKasei Validation Report - Planova TM 20N Filters. 2019. https://planova.ak-bio.com/technical-documents/?per_page=30 (Accessed 2020).
  • AsahiKasei Validation Report - Planova TM BioEX Filters. 2018. https://planova.ak-bio.com/technical-documents/ (Accessed 2020).
  • Zydney, A. L. Perspectives on Integrated Continuous Bioprocessing - Opportunities and Challenges. Current opinion in chemical engineering. 2015, 10, 8–13. DOI: 10.1016/j.coche.2015.07.005.
  • Hongo-Hirasaki, T.; Yamaguchi, K.; Yanagida, K.; Okuyama, K. Removal of Small Viruses (Parvovirus) from IgG Solution by Virus Removal Filter PlanovaTM 20N. J. Memb. Sci. 2006, 278, 3–9. DOI: 10.1016/j.memsci.2005.10.057.
  • Fallahianbijan, F.; Giglia, S.; Carbrello, C.; Zydney, A. L. Use of Fluorescently-Labeled Nanoparticles to Study Pore Morphology and Virus Capture in Virus Filtration Membranes. J. Memb. Sci. 2017, 536, 52–58. DOI: 10.1016/j.memsci.2017.04.066.
  • Bakhshayeshi, M.; Kanani, D. M.; Mehta, A.; van Reis, R.; Kuriyel, R.; Jackson, N.; Zydney, A. L. Dextran Sieving Test for Characterization of Virus Filtration Membranes. J. Memb. Sci. 2011, 379, 239–248. DOI: 10.1016/j.memsci.2011.05.067.
  • Giglia, S.; Bohonak, D.; Greenhalgh, P.; Leahy, A. Measurement of Pore Size Distribution and Prediction of Membrane Filter Virus Retention Using Liquid-Liquid Porometry. J. Memb. Sci. 2015, 476, 399–409. DOI: 10.1016/j.memsci.2014.11.053.
  • Kosiol, P.; Hansmann, B.; Ulbricht, M.; Thom, V. Determination of Pore Size Distributions of Virus Filtration Membranes Using Gold Nanoparticles and Their Correlation with Virus Retention. J. Memb. Sci. 2017, 533, 289–301. DOI: 10.1016/j.memsci.2017.03.043.
  • Ayano, M.; Sawamura, Y.; Hongo-Hirasaki, T.; Nishizaka, T. Direct Visualization of Virus Removal Process in Hollow Fiber Membrane Using an Optical Microscope. Sci. Rep. 2021, 11, 1–9. DOI: 10.1038/s41598-020-78637-z.
  • Nazem-Bokaee, H.; Chen, D.; O’Donnell, S. M.; Zydney, A. L. New Insights into the Performance Characteristics of the Planova-Series Hollow-Fiber Parvovirus Filters Using Confocal and Electron Microscopy. Biotechnol. Bioeng. 2019, 116, 2010–2017. DOI: 10.1002/bit.26991.
  • Adan-Kubo, J.; Tsujikawa, M.; Takahashi, K.; Hongo-Hirasaki, T.; Sakai, K. Microscopic Visualization of Virus Removal by Dedicated Filters Used in Biopharmaceutical Processing: Impact of Membrane Structure and Localization of Captured Virus Particles. Biotechnol. Prog. 2019, 35, 1–11. DOI: 10.1002/btpr.2875.
  • Dishari, S. K.; Micklin, M. R.; Sung, K. J.; Zydney, A. L.; Venkiteshwaran, A.; Earley, J. N. Effects of Solution Conditions on Virus Retention by the Viresolve® NFP Filter. Biotechnol. Prog. 2015, 31, 1280–1286. DOI: 10.1002/btpr.2125.
  • Bao, R. M.; Shibuya, A.; Uehira, T.; Sato, T.; Urayama, T.; Sakai, K.; Yunoki, M. Successful Removal of Porcine Circovirus-1 from Immunoglobulin G Formulated in Glycine Solution Using Nanofiltration. Biologicals. 2018, 51, 32–36. DOI: 10.1016/j.biologicals.2017.10.006.
  • Strauss, D.; Goldstein, J.; Hongo-Hirasaki, T.; Yokoyama, Y.; Hirotomi, N.; Miyabayashi, T.; Vacante, D. Characterizing the Impact of Pressure on Virus Filtration Processes and Establishing Design Spaces to Ensure Effective Parvovirus Removal. Biotechnol. Prog. 2017, 33, 1294–1302. DOI: 10.1002/btpr.2506.
  • Yokoyama, T.; Murai, K.; Murozuka, T.; Wakisaka, A.; Tanifuji, M.; Fujii, N.; Tomono, T. Removal of Small Non-Enveloped Viruses by Nanofiltration. Vox. Sang. 2004, 86, 225–229. DOI: 10.1111/j.0042-9007.2004.00515.x.
  • Lute, S.; Kozaili, J.; Johnson, S.; Kobayashi, K.; Strauss, D . Development of Small-Scale Models to Understand the Impact of Continuous Downstream Bioprocessing on Integrated Virus Filtration. Biotechnol. Prog. 2020, 1–9. DOI: 10.1002/btpr.2962.
  • Bolton, G.; Cabatingan, M.; Rubino, M.; Lute, S.; Brorson, K.; Bailey, M. Normal-Flow Virus Filtration: Detection and Assessment of the Endpoint in Bioprocessing. Biotechnol. Appl. Biochem. 2005, 42, 133. DOI: 10.1042/ba20050056.
  • Kosiol, P.; Kahrs, C.; Thom, V.; Ulbricht, M.; Hansmann, B . Investigation of Virus Retention by Size Exclusion Membranes under Different Flow Regimes. Biotechnol. Prog. 2019, 35. DOI: 10.1002/btpr.2747.
  • Hongo-Hirasaki, T.; Komuro, M.; Ide, S. Effect of Antibody Solution Conditions on Filter Performance for Virus Removal Filter PlanovaTM 20N. Biotechnol. Prog. 2010, 26, 1080–1087. DOI: 10.1002/btpr.415.
  • Nazem-Bokaee, H.; Chen, D.; O’Donnell, S. M.; Zydney, A. L. Visualizing Effects of Protein Fouling on Capture Profiles in the Planova BioEX and 20N Virus Filters. J. Memb. Sci. 2020, 610, 118271. DOI: 10.1016/j.memsci.2020.118271.
  • Wu, L.; Manukyan, L.; Mantas, A.; Mihranyan, A. Nanocellulose-Based Nanoporous Filter Paper for Virus Removal Filtration of Human Intravenous Immunoglobulin. ACS Appl. Nano Mater. 2019, 2, 6352–6359. DOI: 10.1021/acsanm.9b01351.
  • Khan, N. Z.; Parrella, J. J.; Genest, P. W.; Colman, M. S. Filter Preconditioning Enables Representative Scaled-down Modelling of Filter Capacity and Viral Clearance by Mitigating the Impact of Virus Spike Impurities. Biotechnol. Appl. Biochem. 2009, 52, 293. DOI: 10.1042/ba20080133.
  • Lute, S.; Bailey, M.; Combs, J.; Sukumar, M.; Brorson, K. Phage Passage after Extended Processing in Small-Virus-Retentive Filters. Biotechnol. Appl. Biochem. 2007, 47, 141. DOI: 10.1042/ba20060254.
  • Rathore, A. S.; Kumar, V.; Arora, A.; Lute, S.; Brorson, K.; Shukla, A. Mechanistic Modeling of Viral Filtration. J. Memb. Sci. 2014, 458, 96–103. DOI: 10.1016/j.memsci.2014.01.037.
  • Misra, P.; Sinha, A.; Rathore, A. S.; Shukla, A.; Mir, F. Q. A Three Plus Three Parameters Mechanistic Model for Viral Filtration. Biotechnol. Prog. 2017, 33, 1538–1547. DOI: 10.1002/btpr.2523.
  • Jackson, N. B.; Bakhshayeshi, M.; Zydney, A. L.; Mehta, A.; van Reis, R.; Kuriyel, R. Internal Virus Polarization Model for Virus Retention by the Ultipor® VF Grade DV20 Membrane. Biotechnol. Prog. 2014, 30, 856–863. DOI: 10.1002/btpr.1897.
  • Bohonak, D. M.; Mehta, U.; Weiss, E. R.; Voyta, G . Adapting Virus Filtration to Enable Intensified and Continuous Monoclonal Antibody Processing. Biotechnol. Prog. 2020. DOI: 10.1002/btpr.3088.
  • Shirataki, H.; Yokoyama, Y.; Taniguchi, H.; Azeyanagi, M. Analysis of Filtration Behavior Using Integrated Column Chromatography Followed by Virus Filtration. Biotechnol. Bioeng. 2021, 118, 3569–3580. DOI: 10.1002/bit.27840.
  • Tang, A.; Ramos, I.; Newell, K.; Stewart, K. D. A Novel High-Throughput Process Development Screening Tool for Virus Filtration. J. Memb. Sci. 2020, 611, 118330. DOI: 10.1016/j.memsci.2020.118330.
  • Woods, M. A.; Zydney, A. L. Effects of a Pressure Release on Virus Retention with the Ultipor DV20 Membrane. Biotechnol. Bioeng. 2014, 111, 545–551. DOI: 10.1002/bit.25112.
  • LaCasse, D.; Lute, S.; Fiadeiro, M.; Basha, J.; Stork, M.; Brorson, K.; Godavarti, R.; Gallo, C. Mechanistic Failure Mode Investigation and Resolution of Parvovirus Retentive Filters. Biotechnol. Prog. 2016, 32, 959–970. DOI: 10.1002/btpr.2298.
  • Asper, M. Virus Breakthrough after Pressure Release during Virus Retentive Filtration. In Proceedings of the Parenteral Drug Association Virus and TSE Safety Forum; Barcelona, Spain, 2011.
  • Dishari, S. K.; Venkiteshwaran, A.; Zydney, A. L. Probing Effects of Pressure Release on Virus Capture during Virus Filtration Using Confocal Microscopy. Biotechnol. Bioeng. 2015, 112, 2115–2122. DOI: 10.1002/bit.25614.
  • Leisi, R.; Widmer, E.; Gooch, B.; Roth, N. J.; Ros, C. Mechanistic Insights into flow-dependent Virus Retention in Different Nanofilter Membranes. J. Memb. Sci. 2021, 636, 119548. DOI: 10.1016/j.memsci.2021.119548.
  • She, Q.; Wang, R.; Fane, A. G.; Tang, C. Y. Membrane Fouling in Osmotically Driven Membrane Processes: A Review. J. Memb. Sci. 2016, 499, 201–233. DOI: 10.1016/j.memsci.2015.10.040.
  • Marshall, A. D.; Munro, P. A.; Trägårdh, G. The Effect of Protein Fouling in Microfiltration and Ultrafiltration on Permeate Flux, Protein Retention and Selectivity: A Literature Review. Desalination. 1993, 91, 65–108. DOI: 10.1016/0011-9164(93)80047-Q.
  • Fane, A. G.; Fell, C. J. D. A Review of Fouling and Fouling Control in Ultrafiltration. Desalination. 1987, 62, 117–136. DOI: 10.1016/0011-9164(87)87013-3.
  • Bieberbach, M.; Kosiol, P.; Seay, A.; Bennecke, M.; Hansmann, B.; Hepbildikler, S.; Thom, V. Investigation of Fouling Mechanisms of Virus Filters during the Filtration of Protein Solutions Using a High Throughput Filtration Screening Device. Biotechnol. Prog. 2019, 35, 1–10. DOI: 10.1002/btpr.2776.
  • Bohonak, D. M.; Zydney, A. L. Compaction and Permeability Effects with Virus Filtration Membranes. J. Memb. Sci. 2005, 254, 71–79. DOI: 10.1016/j.memsci.2004.12.035.
  • Arkhangelsky, E.; Gitis, V. Effect of Transmembrane Pressure on Rejection of Viruses by Ultrafiltration Membranes. Sep. Purif. Technol. 2008, 62, 619–628. DOI: 10.1016/j.seppur.2008.03.013.
  • Fan, R.; Namila, F.; Sansongko, D.; Wickramasinghe, S. R.; Jin, M.; Kanani, D.; Qian, X. The Effects of Flux on the Clearance of Minute Virus of Mice during Constant Flux Virus Filtration. Biotechnol. Bioeng. 2021, 118, 3511–3521. DOI: 10.1002/bit.27778.
  • David, L.; Niklas, J.; Budde, B.; Lobedann, M.; Schembecker, G. Continuous Viral Filtration for the Production of Monoclonal Antibodies. Chem. Eng. Res. Des. 2019, 152, 336–347. DOI: 10.1016/j.cherd.2019.09.040.

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