The potential of hydrodynamic damage to animal cells of industrial relevance: Current understanding

Cytotechnology

Volumn 63, Issue 5, 2011, Pages 445-460

  Hu, Weiwei ^a   Berdugo, Claudia ^b   Chalmers, Jeffrey J ^c  

^a BIOGEN   (United States)

^b Scientist/Research and Development   (United States)

^c Ohio State University   (United States)

Author keywords

Agitation; Animal cell culture; Hydrodynamic forces; Scale up; Shear sensitivity; Sparging

Indexed keywords

ANIMAL CELL; BIOREACTOR; CELL CULTURE; CELL DAMAGE; CELL DENSITY; HYDRODYNAMICS; NONHUMAN; REVIEW; SCALE UP; SPARGING;

ANIMALIA;

EID: 84655167606     PISSN: 09209069     EISSN: 15730778     Source Type: Journal    
DOI: 10.1007/s10616-011-9368-3     Document Type: Review

References (102)

1. Aloi LE, Cherry RS (1996) Cellular response to agitation characterized by energy dissipation at the impeller tip. Chem Eng Sci 51:1523-1529
2. Al-Rubeai M, Emery AN, Chalder S, Goldman MH (1993) A flow cytometric study of hydrodynamic damage to mammalian cells. J Biotechnol 31:161-177
3. Assirelli M, Bujalski W, Eaglesham A, Nienow AW (2008) Macro-and micromixing studies in an unbaffled vessel agitated by a Rushton turbine. Chem Eng Sci 63:35-46 (Pubitemid 350101461)
4. Augenstein DC, Sinskey AJ, Wang DIC (1971) Effect of shear on the death of two strains of mammalian tissue cells. Biotechnol Bioeng 13:409-418
5. Barbosa MJ, Hadiyanto, Wijffels RH (2004) Overcoming shear stress of microalgae cultures in sparged photobioreactors. Biotechnol Bioeng 85:78-85 (Pubitemid 38090132)
6. Bavarian F, Fan LS, Chalmers JJ (1991) Microscopic visualization of insect cell-bubble interactions I: Rising bubbles, air-medium, and the foam layer. Biotechnol Prog 7:140-15p
7. Bluestein M, Mockros LF (1969) Hemolytic effects of energy dissipation in flowing blood. Med Biol Eng 7:1-6
8. Boulton-Stone JM, Blake JR (1993) Gas bubbles bursting at a free surface. J Fluid Mech 254:103-111
9. Boychyn M, Doyle W, Bulmer M, More J, Hoare M (2000) Laboratory scaledown of protein purification processes involving fractional precipitation and centrifugal recovery. Biotechnol Bioeng 69:1-1p (Pubitemid 30418256)
10. Boychyn M, Yim SS, Ayazi Shamlou P, Bulmer M, More J, Hoare M (2001) Characterization of flow intensity in continuous centrifuges for the development of laboratory mimics. Chem Eng Sci 56:4759-477p (Pubitemid 32863492)
11. Boychyn M, Yim SS, Bulmer M, More J, Bracewell DG, Hoare M (2004) Performance prediction of industrial centrifuges using scale-down models. Bioprocess Biosyst Eng 26:385-391
12. Chattopadhyay D, Rathman J, Chalmers JJ (1995a) The protective effect of specific medium additives with respect to bubble rupture. Biotechnol Bioeng 45:473-48p
13. Chattopadhyay D, Rathman J, Chalmers JJ (1995b) Thermodynamic approach to explain cell adhesion to gas-medium interfaces. Biotechnol Bioeng 48:649-658
14. Cherry RS, Papoutsakis ET (1986) Hydrodynamic effects on cells in agitated tissue culture reactors. Bioprocess Eng 1:81-89
15. Cherry RS, Papoutsakis ET (1988) Physical mechanisms of cell damage in microcarrier bioreactors. Biotechnol Bioeng 32:1001-1014
16. Cherry RS, Papoutsakis ET (1989) Hydrodynamic effects on cells in agitated tissue culture reactors. Bioprocess Eng 1:29-41
17. Chisti Y (2000) Animal-cell damage in sparged bioreactors. TIBTECH 18:420-432
18. Clay JD, Koelling KW (1997) Molecular degradation of concentrated polystyrene solutions in a fast transient extensional flow. Polym Eng Sci 37:789-80p (Pubitemid 127607750)
19. Crespi CL, Thilly WG (1981) Continuous cell propagation using low-charge microcarriers. Biotechnol Bioeng 3:983-993
20. Costes J, Couderc JP (1988) Influence of the size of units -II spectral analysis and scales of turbulence. Chem Eng Sci 43:2765-2772
21. Croughan MS, Hamel JF, Wang DIC (1987) Hydrodynamic effect on animal cells grown in microcarrier cultures. Biotechnol Bioeng 29:130-141
22. Croughan MS, Sayre ES, Wang DIC (1989) Viscous reduction of turbulent damage in animal cell cultures. Biotechnol Bioeng 33:862-872 (Pubitemid 19062696)
23. Cutter LA (1966) Flow and turbulence in a stirred tank. AICHE J 12:35-4p
24. Fan LS, Tsuchiya K (1990) Bubble wake dynamics in liquids and liquid-solid suspensions. Butterworth Heinemann, Boston
25. Garcia-Briones MA, Chalmers JJ (1994) Flow parameters associated with hydrodynamic cell injury. Biotechnol Bioeng 44:1089-1098 (Pubitemid 24331659)
26. Garcia-Briones M, Brodkey R, Chalmers J (1994) Computer simulations of the rupture of a gas bubble at a gas-liquid interface and its implications in animal cell damage. Chem Eng Sci 49:2301-232p (Pubitemid 281059)
27. Gigout A, Buschmann MD, Jolicoeur M (2008) The fate of pluronic F-68 in chondrocytes and CHO cells. Biotechnol Bioeng 100:975-987
28. Godoy-Silva R, Mollet M, Chalmers JJ (2009a) Evaluation of the effect of chronic hydrodynamic stresses on cultures of suspended CHO-6E6 cells. Biotechnol Bioeng 102:1119-113p
29. Godoy-Silva R, Chalmers JJ, Casnocha SA, Bass LA, Ma N (2009b) Physiological response of CHO cells to repetivtive hydrodynamic stress. Biotechnol Bioeng 103:1103-1117
30. Godoy-Silva R, Berdogo C, Chalmers JJ (2010) Aeration, mixing, and hydrodynamics in bioreactors. In: Flickinger M (ed) The encyclopedia of industrial biotechnology: Bioprocess, bioseparation, and cell technology. Wiley, New York
31. Gregoriades N, Clay J, Ma N, Koelling K, Chalmers JJ (2000) Cell damage of microcarrier cultures as a function of local energy dissipation created by a rapid extensional flow. Biotechnol Bioeng 69:171-182 (Pubitemid 30430088)
32. Hirtenstein MD, Clark JM (1980) Critical parameters in the microcarrier cultures of animal cells. Dev Biol Stand 46:117-124
33. Hoh JH, Schoenenberger CA (1994) Surface morphology and mechanical properties of MDCK monolayers by atomic force microscopy. J Cell Sci 107:1105-1114 (Pubitemid 24177313)
34. Hu W, Rathman JJ, Chalmers JJ (2008) An investigation of small-molecule surfactants to potentially replace pluronic F-68 for reducing bubble-associated cell damage. Biotechnol Bioeng 101:119-127
35. Huang YM, Hu W, Rustandi E, Shen V, Yusuf-Makagiansar H, Ryll T (2010) Maximizing productivity of CHO cell based fed-batch culture using chemically defined media conditions and typical manufacturing equipment. Biotechnol Prog 26:1400-141p
36. Hutchinson N, Bingham N, Murrell N, Farid S, Hoare M (2006) Shear stress analysis of mammalian cell suspensions for prediction of industrial centrifugation and its verification. Biotechnol Bioeng 95:483-491 (Pubitemid 44495383)
37. Joosten CE, Shuler ML (2003) Effect of culture conditions on the degree of sialylation of a recombinant glycoprotein expressed in insect cells. Biotechnol Prog 19:739-749 (Pubitemid 36715116)
38. Joshi JB, Elias CB, Patole MS (1996) Role of hydrodynamic shear in the cultivation of animal, plant and microbial cells. Chem Eng Sci 62:121-141
39. Kao YH, Hewitt DP, Terxler-Schmidt M, Laird MW (2010) Mechanism of antibody reduction in cell culture production processes. Biotechnol Bioeng 107(4):622-632
40. Katinger HWD, Scheirer W, Kromer E (1979) Bubble column reactor for mass propagation of animal cells in suspension culture. Ger Chem Eng 2:31-38
41. Keane JT, Ryan D, Gray PP (2003) Effect of shear stress on expression of a recombinant protein by Chinese hamster ovary cells. Biotechnol Bioeng 81:211-22p (Pubitemid 36077297)
42. Kioukia N, Nienow AW, Al-Rubeai M, Emery AN (1992) The impact of fluid dynamics on the biological performance of free suspension animal cell culture: Further studies. Food Bioprod Proc (Tans I Chem E, Part C) 70:143-148
43. Kioukia N, Nienow AW, Al-Rubeai M, Emery AN (1996) Influnce of agitation and sparging on the growth rate and infection of insect cells in bioreactors and a comparison with hybridoma culture. Biotechnol Prog 12:779-785 (Pubitemid 27015833)
44. Kresta S (1998) Turbulence in stirred tanks: Anisotropic, approximate, and applied. Can J Chem Eng 76:563-576 (Pubitemid 28560793)
45. Kunas KT, Papoutsakis ET (1990) Damage mechanisms of suspended animal cells in agitated bioreactors with and without bubble entrainment. Biotechnol Bioeng 36:476-483 (Pubitemid 20283272)
46. Langheinrich C, Nienow AW (1999) Control of pH in large scale, free suspension animal cell bioreactors: Alkali addition and pH excursions. Biotechnol Bioeng 66:171-179 (Pubitemid 30010341)
47. Levy MS, Collins SS, Yim SS, Ward JM, Titchener-Hooker N, Shamlou PA, Dunnill P (1999a) Effect of shear on plasmid DNA solution. Bioprocess Eng 20:7-13
48. Levy MS, Ciccolini LAS, Yim SSS, Tsai JT, Titchener-Hooker N, Ayazi Shamlou P, Dunnill P (1999b) The effects of material properties and fluid flow intensity on plasmid DNA recovery during cell lysis. Chem Eng Sci 54:3171-3178 (Pubitemid 29419161)
49. Li YSJ, Haga JH, Chien S (2005) Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech 38:1949-1971 (Pubitemid 41111740)
50. Li F, Hashimura Y, Pendleton R, Harms J, Collins E, Lee B (2006) A system approach for scale-down model development and characterization of commercial cell culture processes. Biotechnol Prog 22:696-703 (Pubitemid 43877437)
51. Luan YT, Wang W, Nolan R, Drapeau D (2006) Defined medium development for high yielding mammalian cell culture processes. In: IBC & bioprocess international conference, Nov 2006, San Francisco, CA
52. Ma N, Koelling KW, Chalmers JJ (2002) Fabrication and use of a transient contractional flow device to quantify the sensitivity of mammalian and insect cells to hydrodynamic forces. Biotechnol Bioeng 80:428-437 (Pubitemid 35230937)
53. Ma N, Chalmers JJ, Aunins JG, Zhou W, Xie L (2004) Quantitative studies of cell-bubble interactions and cell damage at different Pluronic F-68 and cell concentrations. Biotechnol Prog 20:1183-1191 (Pubitemid 39059632)
54. MacIntyre F (1972) Flow patterns in breaking bubbles. J Fluid Mech 77:5211-5228
55. Markopoulos J, Kontogeorgaki E (1995) Vortex depth in unbaffled single and multiple impeller agitated vessels. Chem Eng Technol 18:68-74
56. McCoy R, HoareM(2009) Ultra scale-down studies of the effect of shear on cell quality: Processing of human cell line for cancer vaccine therapy. Biotechnol Prog 25:1448-1458
57. McCoy R, Ward S, Hoare M (2010) Sub-population analysis of human cancer vaccine cells-ultra scale-down characterization of response to shear.BiotechnolBioeng 106:584-595
58. McDowell CL, Papoutsakis ET (1998) Increased agitation intensity increases CD13 receptor surface content and mRNA levels, and alters the metabolism of HL60 cells cultured in a stirred tank bioreactor. Biotechnol Bioeng 60:239-25p (Pubitemid 28432367)
59. McQueen A, Bailey JE (1989) Influence of serum level, cell line, flow type and viscosity on flow-induced lysis of suspended mammalian cells. Biotechnol Lett 11:531-536
60. Meier SJ, Hatton TA, Wang DIC (1999) Cell death from bursting bubbles: Role of cell attachment to rising bubbles in sparged reactors. Biotechnol Bioeng 62:468-478 (Pubitemid 29052882)
61. Michaels JD, Papoutsakis ET (1991) Polyvinyl alcohol and polyethylene glycol as protectants against fluid-mechanical injury of freely-suspended animal cells (CRL8018). J Biotechnol 19:241-258
62. Michaels JD, Kunas KT, Papoutsakis ET (1992) Fluidmechanical damage of freely-suspended animal cells in agitated bioreactors: Effects of dextran, derivatized celluloses and polyvinyl alcohol. Chem Eng Commun 118:341-36p
63. Michaels J, Nowak JE, Mallik AK, Koczo K, Wasan DT, Papoutsakis ET (1995) Analysis of cell-to-bubble attachment in sparged bioreactors in the presence of cell-protecting additives. Biotechnol Bioeng 47:407-419
64. Mollet M, Ma N, Zhao Y, Brodkey R, Taticek R, Chalmers JJ (2004) Bioprocess equipment: Characterization of energy dissipation rate and its potential to damage cells. Biotechnol Prog 20:1437-1448 (Pubitemid 39351328)
65. Mollet M, Godoy-Silva R, Berdugo C, Chalmers JJ (2007) Acute hydrodynamic forces and apoptosis: A complex question. Biotechnol Bioeng 98:772-788 (Pubitemid 350032682)
66. Mollet M, Godoy-Silva R, Berdugo C, Chalmers JJ (2008) Computer simulations of the energy dissipation rate in a fluorescence activated cell sorter: Implications to cells. Biotechnol Bioeng 100:260-272 (Pubitemid 351758169)
67. 2 removal in large-scale fed-batch cultures. Biotechnol Prog 19:45-51 (Pubitemid 36219302)
68. Motobu M, Wang P-C, Matsumura M (1998) Effect of shear stress on recombinant Chinese hamster ovary cells. J Ferment Bioeng 85:190-195 (Pubitemid 28207549)
69. Murhammer DW, Goochee CF (1990) Structural features of nonionic polyglycol polymer molecules responsible for the protective effect in sparged animal cell bioreactors. Biotechnol Prog 6:142-148
70. Neal G, Christie J, Keshavarz-Moore E, Shamlou PA. (2003) Ultra scale-down approach for the prediction of full-scale recovery of ovine polycholonal immunoglobulins used in the manufacture of snake vemon-specific Fab fragment. Biotechnol Bioeng 81(2):149-157 (Pubitemid 36077291)
71. Niagam P (2006) Interaction of water-soluble surfactants with self-assembled lipid monolayers at the vapor-liquid interface: Equilibrium and dynamic phenomena. PhD thesis. The Ohio State University
72. Nienow AW (2006) Reactor engineering in large scale animal cell culture. Cytotechnology 50:9-33
73. Okamoto Y, Nishikawa M, Hashimoto K (1981) Energy Dissipation Rate Distribution in Mixing Vessels and Soild-Liquid Mass Transfer. Int Chem Eng 21:88-94
74. Oh SKW, Nienow AW, Al-Rubeai M, Emery AN (1989) The effects of agitation intensity with and without continuous sparging on the growth and antibody production of hybridoma cells. J Biotechnol 12:45-62 (Pubitemid 19247570)
75. Oh SKW, Nienow AW, Al-Rubeai M, Emery AN (1992) Further studies of the culture of mouse hybridomas in an agitated bioreactor with and without continuous sparging. J Biotechnol 22:245-27p
76. Palomares LA, González M, Ramírez OT (2000) Evidence of Pluronic F-68 direct interaction with insect cells: Impact on shear protection, recombinant protein, and baculovirus production. Enzym Microb Technol 26:324-331 (Pubitemid 30122397)
77. Ramirez OT, Mutharasan R (1990) The role of the plasma membrane fluidity on the shear sensitivity of hybridoma growth under hydrodynamic stress. Biotechnol Bioeng 36:911-92p (Pubitemid 20365649)
78. Ranjan V, Waterbury R, Xiao Z, Diamond SL (1995) Fluid shear stress induction of the transcriptional activator c-fos in human and bovine endothelial cells, Hela, and Chinese hamster ovary cells. Biotechnol Bioeng 49:383-39p (Pubitemid 26039009)
79. Senger R, Karim MN (2003) Effect of shear stress on intrinsic CHO culture state and glycosylation of recombinant tissue-type plasminogen activator protein. Biotechnol Prog 19:1199-1209 (Pubitemid 37007602)
80. Swim HE, Parker RF (1960) Effect of Pluronic F68 on growth of fibroblasts in suspension on rotary shaker. Proc Soc Exp Biol Med 103:252-254
81. Tatterson GB, Yuan HS, Brodkey BS (1980) Stereoscopic visualization of the flows for pitched blade turbines. Chem Eng Sci 35:1369-1375
82. Telling RC, Elsworth R (1965) Submerged culture of hamster kidney cells in a stainless steel vessel. Biotechnol Bioeng 7:417-434
83. Thomas CR, Al-Rubeai M, Zhang Z (1994) Prediction of mechanical damage to animal cells in turbulence. Cytotechnol 15:329-335
84. Trexler-Schmidt M, Sargis S, Chiu J, Sze-Khoo S, Mun M, Kao YH, Laird MW (2010) Identification and prevention of antibody disulfide bond reduction during cell culture manufacturing. Biotechnol Bioeng 106:452-461
85. Trinh K, Garcia-Briones M, Hink F, Chalmers JJ (1994) Quantification of damage to suspended insect cells as a result of bubble rupture. Biotechnol Bioeng 43:37-45 (Pubitemid 24001734)
86. Vakili MH, Esfahanny MN (2009) CFD analysis of turbulence in a baffled stirred tank, a three-compartment model. Chem Eng Sci 64:351-362
87. Van der Pol LA, Beeksma I, Tramper J (1995) Polyethylene glycol as protectant against damage caused by sparging for hybridoma suspension cells in a bubble column. Enzym Microb Technol 17:401-407
88. Van't Riet K, Smith JM (1975) The trailing vortex system produced by Rushton turbine agitators. Chem Eng Sci 30:1093-1105
89. Varley J, Birth J (1999) Reactor design for large scale suspension animal cell culture. Cytotechnology 29:177-205 (Pubitemid 29207781)
90. Venkat R, Stock R, Chalmers JJ (1996) Study of hydrodynamics in microcarrier culture spinner vessels: A particle tracking velocimetry approach. Biotechnol Bioeng 49:456-466 (Pubitemid 26039017)
91. Vickroy B, Lorenz K, Kelly W (2007) Modeling shear damage to suspended CHO cells during cross-flow filtration. Biotechnol Prog 23:194-199 (Pubitemid 46293504)
92. Wernersson ES, Trägårdh C (1999) Scale-up of Rushton turbine-agitated tanks. Chem Eng Sci 54:4245-4256 (Pubitemid 29424920)
93. Westoby M, Rogers JK, Haverstock R, Romero J, Pieracci J (2011) Modeling industrial centrifugation of mammalian cell culture using a capillary based scale-down system. Biotechnol Bioeng 108:989-998
94. Wu H, Patterson GK (1989) Laser-Doppler measurements of turbulent flow parameters in a stirred mixer. Chem Eng Sci 44:2207-2221 (Pubitemid 20611454)
95. Wurm FM(2004) Production of recombinant protein therapeutics in cultivated ammalian cells. Nat Biotechnol 22:1393-1398 (Pubitemid 39482858)
96. Xing Z, Kenty BM, Li ZJ, Lee SS (2009) Scale-up analysis for a CHO cell culture process in large-scale bioreactors. Biotechnol Bioeng 103:733-746
97. Zhang Z, Thomas CR (1993) Modeling of animal cell damage in turbulent flows. In: Nienow AW (eds) Proc. 3rd int. conf. on bioreactor and bioprocesses fluid dynamics. Mechanical Engineering Publications Ltd., London, pp 475-482. ISBN 0852988737
98. Zhang Z, Ferenczi MA, Thomas CR (1992) A micromanipulation technique with theoretical cell model for determining mechanical properties of single mammalian cells. Chem Eng Sci 47:1347-1354 (Pubitemid 23560282)
99. Zhou G, Kresta SM (1996a) Distribution of energy dissipation between convective and turbulent flow for three frequently used impellers. Trans I Chem E 74:379-389 (Pubitemid 126494598)
100. Zhou G, Kresta SM (1996b) Impact of tank geometry on the maximum turbulence energy dissipation rate for impellers. AIChE J 42:2476-249p (Pubitemid 126452361)
101. 2 and osmolality on growth of CHO cells and production of antibody-fusion protein B1: A case study. Biotechnol Prog 21:70-77 (Pubitemid 40218473)
102. Zhu Y, Cuenca JV, Zhou W, Varma A (2008) NS0 cell damage by high gas velocity sparging in protein-free and cholesterol-free cultures. Biotechnol Bioeng 101:751-76p