Skip to main content
SpringerLink
Log in

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

  • Review
  • Published:
Cytotechnology Aims and scope Submit manuscript

Abstract

Suspension animal cell culture is now routinely scaled up to bioreactors on the order of 10,000 L, and greater, to meet commercial demand. However, the concern of the ‘shear sensitivity’ of animal cells still remains, not only within the bioreactor, but also in the downstream processing. As the productivities continue to increase, titer of ~10 g/L are now reported with cell densities greater than 2 × 107 cells/mL. Such high, and potentially higher cell densities will inevitably translate to increased demand in mass transfer and mixing. In addition, achieving productivity gains in both the upstream stage and downstream processes can subject the cells to aggressive environments such as those involving hydrodynamic stresses. The perception of ‘shear sensitivity’ has historically put an arbitrary upper limit on agitation and aeration in bioreactor operation; however, as cell densities and productivities continue to increase, mass transfer requirements can exceed those imposed by these arbitrary low limits. Therefore, a better understanding of how animal cells, used to produce therapeutic products, respond to hydrodynamic forces in both qualitative and quantitative ways will allow an experimentally based, higher, “upper limit” to be created to guide the design and operation of future commercial, large scale bioreactors. With respect to downstream hydrodynamic conditions, situations have already been achieved in which practical limits with respect to hydrodynamic forces have been experienced. This review mainly focuses on publications from both the academy and industry regarding the effect of hydrodynamic forces on industrially relevant animal cells, and not on the actual scale-up of bioreactors. A summary of implications and remaining challenges will also be presented.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aloi LE, Cherry RS (1996) Cellular response to agitation characterized by energy dissipation at the impeller tip. Chem Eng Sci 51:1523–1529

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Barbosa MJ, Hadiyanto, Wijffels RH (2004) Overcoming shear stress of microalgae cultures in sparged photobioreactors. Biotechnol Bioeng 85:78–85

  • 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 7:140–150

    Article  CAS  Google Scholar 

  • Bluestein M, Mockros LF (1969) Hemolytic effects of energy dissipation in flowing blood. Med Biol Eng 7:1–6

    Article  CAS  Google Scholar 

  • Boulton-Stone JM, Blake JR (1993) Gas bubbles bursting at a free surface. J Fluid Mech 254:103–111

    Article  Google Scholar 

  • 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 69:1–10

    Article  CAS  Google Scholar 

  • 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 56:4759–4770

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chattopadhyay D, Rathman J, Chalmers JJ (1995a) The protective effect of specific medium additives with respect to bubble rupture. Biotechnol Bioeng 45:473–480

    Article  CAS  Google Scholar 

  • Chattopadhyay D, Rathman J, Chalmers JJ (1995b) Thermodynamic approach to explain cell adhesion to gas-medium interfaces. Biotechnol Bioeng 48:649–658

    Article  CAS  Google Scholar 

  • Cherry RS, Papoutsakis ET (1986) Hydrodynamic effects on cells in agitated tissue culture reactors. Bioprocess Eng 1:81–89

    Article  Google Scholar 

  • Cherry RS, Papoutsakis ET (1988) Physical mechanisms of cell damage in microcarrier bioreactors. Biotechnol Bioeng 32:1001–1014

    Article  CAS  Google Scholar 

  • Cherry RS, Papoutsakis ET (1989) Hydrodynamic effects on cells in agitated tissue culture reactors. Bioprocess Eng 1:29–41

    Article  Google Scholar 

  • Chisti Y (2000) Animal-cell damage in sparged bioreactors. TIBTECH 18:420–432

    CAS  Google Scholar 

  • Clay JD, Koelling KW (1997) Molecular degradation of concentrated polystyrene solutions in a fast transient extensional flow. Polym Eng Sci 37:789–800

    Article  CAS  Google Scholar 

  • Crespi CL, Thilly WG (1981) Continuous cell propagation using low-charge microcarriers. Biotechnol Bioeng 3:983–993

    Article  Google Scholar 

  • Costes J, Couderc JP (1988) Influence of the size of units - II spectral analysis and scales of turbulence. Chem Eng Sci 43:2765–2772

    Google Scholar 

  • Croughan MS, Hamel JF, Wang DIC (1987) Hydrodynamic effect on animal cells grown in microcarrier cultures. Biotechnol Bioeng 29:130–141

    Article  CAS  Google Scholar 

  • Croughan MS, Sayre ES, Wang DIC (1989) Viscous reduction of turbulent damage in animal cell cultures. Biotechnol Bioeng 33:862–872

    Article  CAS  Google Scholar 

  • Cutter LA (1966) Flow and turbulence in a stirred tank. AICHE J 12:35–40

    Google Scholar 

  • Fan LS, Tsuchiya K (1990) Bubble wake dynamics in liquids and liquid–solid suspensions. Butterworth Heinemann, Boston

    Google Scholar 

  • Garcia-Briones MA, Chalmers JJ (1994) Flow parameters associated with hydrodynamic cell injury. Biotechnol Bioeng 44:1089–1098

    Article  CAS  Google Scholar 

  • 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 49:2301–2320

    Article  CAS  Google Scholar 

  • Gigout A, Buschmann MD, Jolicoeur M (2008) The fate of pluronic F-68 in chondrocytes and CHO cells. Biotechnol Bioeng 100:975–987

    Article  CAS  Google Scholar 

  • 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 102:1119–1130

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • Hirtenstein MD, Clark JM (1980) Critical parameters in the microcarrier cultures of animal cells. Dev Biol Stand 46:117–124

    Google Scholar 

  • Hoh JH, Schoenenberger CA (1994) Surface morphology and mechanical properties of MDCK monolayers by atomic force microscopy. J Cell Sci 107:1105–1114

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 26:1400–1410

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Keane JT, Ryan D, Gray PP (2003) Effect of shear stress on expression of a recombinant protein by Chinese hamster ovary cells. Biotechnol Bioeng 81:211–220

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kresta S (1998) Turbulence in stirred tanks: anisotropic, approximate, and applied. Can J Chem Eng 76:563–576

    Article  CAS  Google Scholar 

  • Kunas KT, Papoutsakis ET (1990) Damage mechanisms of suspended animal cells in agitated bioreactors with and without bubble entrainment. Biotechnol Bioeng 36:476–483

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Li YSJ, Haga JH, Chien S (2005) Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech 38:1949–1971

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • MacIntyre F (1972) Flow patterns in breaking bubbles. J Fluid Mech 77:5211–5228

    CAS  Google Scholar 

  • Markopoulos J, Kontogeorgaki E (1995) Vortex depth in unbaffled single and multiple impeller agitated vessels. Chem Eng Technol 18:68–74

    Article  CAS  Google Scholar 

  • McCoy R, Hoare M (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

    Article  CAS  Google Scholar 

  • McCoy R, Ward S, Hoare M (2010) Sub-population analysis of human cancer vaccine cells—ultra scale-down characterization of response to shear. Biotechnol Bioeng 106:584–595

    Article  CAS  Google Scholar 

  • 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 60:239–250

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Michaels JD, Kunas KT, Papoutsakis ET (1992) Fluid-mechanical damage of freely-suspended animal cells in agitated bioreactors: effects of dextran, derivatized celluloses and polyvinyl alcohol. Chem Eng Commun 118:341–360

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mollet M, Godoy-Silva R, Berdugo C, Chalmers JJ (2007) Acute hydrodynamic forces and apoptosis: a complex question. Biotechnol Bioeng 98:772–788

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mostafa SS, Gu X (2003) Strategies for improved dCO2 removal in large-scale fed-batch cultures. Biotechnol Prog 19:45–51

    Article  CAS  Google Scholar 

  • Motobu M, Wang P-C, Matsumura M (1998) Effect of shear stress on recombinant Chinese hamster ovary cells. J Ferment Bioeng 85:190–195

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

  • Nienow AW (2006) Reactor engineering in large scale animal cell culture. Cytotechnology 50:9–33

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 22:245–270

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ramirez OT, Mutharasan R (1990) The role of the plasma membrane fluidity on the shear sensitivity of hybridoma growth under hydrodynamic stress. Biotechnol Bioeng 36:911–920

    Article  CAS  Google Scholar 

  • 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 49:383–390

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Tatterson GB, Yuan HS, Brodkey BS (1980) Stereoscopic visualization of the flows for pitched blade turbines. Chem Eng Sci 35:1369–1375

    Article  CAS  Google Scholar 

  • Telling RC, Elsworth R (1965) Submerged culture of hamster kidney cells in a stainless steel vessel. Biotechnol Bioeng 7:417–434

    Article  Google Scholar 

  • Thomas CR, Al-Rubeai M, Zhang Z (1994) Prediction of mechanical damage to animal cells in turbulence. Cytotechnol 15:329–335

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vakili MH, Esfahanny MN (2009) CFD analysis of turbulence in a baffled stirred tank, a three-compartment model. Chem Eng Sci 64:351–362

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Van’t Riet K, Smith JM (1975) The trailing vortex system produced by Rushton turbine agitators. Chem Eng Sci 30:1093–1105

    Article  Google Scholar 

  • Varley J, Birth J (1999) Reactor design for large scale suspension animal cell culture. Cytotechnology 29:177–205

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vickroy B, Lorenz K, Kelly W (2007) Modeling shear damage to suspended CHO cells during cross-flow filtration. Biotechnol Prog 23:194–199

    Article  CAS  Google Scholar 

  • Wernersson ES, Trägårdh C (1999) Scale-up of Rushton turbine-agitated tanks. Chem Eng Sci 54:4245–4256

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wu H, Patterson GK (1989) Laser-Doppler measurements of turbulent flow parameters in a stirred mixer. Chem Eng Sci 44:2207–2221

    Google Scholar 

  • Wurm FM (2004) Production of recombinant protein therapeutics in cultivated ammalian cells. Nat Biotechnol 22:1393–1398

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Zhou G, Kresta SM (1996b) Impact of tank geometry on the maximum turbulence energy dissipation rate for impellers. AIChE J 42:2476–2490

    Article  CAS  Google Scholar 

  • Zhu MM, Goyal A, Rank DL, Gupta SK, VandenBoom T, Lee SS (2005) Effects of elevated pCO2 and osmolality on growth of CHO cells and production of antibody-fusion protein B1: a case study. Biotechnol Prog 21:70–77

    Article  Google Scholar 

  • 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 101:751–760

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cell Culture Development, Biogen Idec Inc., 5000 Davis Drive, RTP, NC, 27709, USA

    Weiwei Hu

  2. William G. Lowrie Department of Chemical and Biomolecular Engineering, The Ohio State University, 140 West 19th Ave., Columbus, OH, 43210, USA

    Jeffrey J. Chalmers

  3. Scientist / Research & Development, BD Biosciences, 54 Loveton Circle, Sparks, MD, 21152, USA

    Claudia Berdugo

Authors
  1. Weiwei Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudia Berdugo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffrey J. Chalmers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeffrey J. Chalmers.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hu, W., Berdugo, C. & Chalmers, J.J. The potential of hydrodynamic damage to animal cells of industrial relevance: current understanding. Cytotechnology 63, 445–460 (2011). https://doi.org/10.1007/s10616-011-9368-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10616-011-9368-3

Keywords

Search

Navigation