1,388
Views
63
CrossRef citations to date
0
Altmetric
Review Article

Recent advances in mechanical characterisation of biofilm and their significance for material modelling

, , , &
Pages 145-171 | Received 01 Dec 2011, Accepted 21 Mar 2012, Published online: 29 May 2012

References

  • Abu-Lail LI, Liu Y, Atabek A, Camesano TA. 2007. Quantifying the adhesion and interaction forces between Pseudomonas aeruginosa and natural organic matter. Environ Sci Technol 41: 8031–8037.
  • Aggarwal S, Hozalski RM. 2010. Determination of biofilm mechanical properties from tensile tests performed using a micro-cantilever method. Biofouling 26: 479–486.
  • Aggarwal S, Poppele EH, Hozalski RM. 2010. Development and testing of a novel microcantilever technique for measuring the cohesive strength of intact biofilms. Biotechnol Bioeng 105: 924–934.
  • Ahimou F, Semmens MJ, Novak PJ, Haugstad G. 2007. Biofilm cohesiveness measurement using a novel atomic force microscopy methodology. Appl Environ Microbiol 73: 2897–2904.
  • Alfa MJ, Howie R. 2009. Modeling microbial survival in buildup biofilm for complex medical devices. BMC Infect Dis 9: 56.
  • Alpkvist E, Klapper I. 2007. A multidimensional multispecies continuum model for heterogeneous biofilm development. Bull Math Biol 69: 765–789.
  • Alpkvist E, Picioreanu C, van Loosdrecht MC, Heyden A. 2006. Three-dimensional biofilm model with individual cells and continuum EPS matrix. Biotechnol Bioeng 94: 961–979.
  • Aravas N, Laspidou CS. 2008. On the calculation of the elastic modulus of a biofilm streamer. Biotechnol Bioeng 101: 196–200.
  • Arce FT, Carlson R, Monds J, Veeh R, Hu FZ, Stewart PS, Lal R, Ehrlich GD, Avci R. 2009. Nanoscale structural and mechanical properties of nontypeable Haemophilus influenzae biofilms. J Bacteriol 191: 2512–2520.
  • Auerbach ID, Sorensen C, Hansma HG, Holden PA. 2000. Physical morphology and surface properties of unsaturated Pseudomonas aeruginosa biofilms. J Bacteriol 182: 3809–3815.
  • Bayoudh S, Othmane A, Mora L, Ben Ouada H. 2009. Assessing bacterial adhesion using DLVO and XDLVO theories and the jet impingement technique. Colloids Surf B Biointerfaces 73: 1–9.
  • Bayoudh S, Ponsonnet L, Ben Quada H, Bakhrouf A, Othmane A. 2005. Bacterial detachment from hydrophilic and hydrophobic surfaces using a microjet impingement. Colloid Surface A 266: 160–167.
  • Beech IB. 1996. The potential use of atomic force microscopy for studying corrosion of metals in the presence of bacterial biofilms - an overview. Int Biodeter Biodegr 37: 141–149.
  • Beech IB, Smith JR, Steele AA, Penegar I, Campbell SA. 2002. The use of atomic force microscopy for studying interactions of bacterial biofilms with surfaces. Colloid Surface B 23: 231–247.
  • Binnig G, Quate CF, Gerber C. 1986. Atomic force microscope. Phys Rev Lett 56: 930–933.
  • Bjarnsholt T. 2011. Biofilm infections. New York: Springer.
  • Böl M. 2010. Micromechanical modelling of skeletal muscles: from the single fibre to the whole muscle. Arch Appl Mech 80: 557–567.
  • Böl M, Möhle RB, Haesner M, Neu TR, Horn H, Krull R. 2009. 3D finite element model of biofilm detachment using real biofilm structures from CLSM data. Biotechnol Bioeng 103: 177–186.
  • Böl M, Reese S. 2006. Finite element modelling of rubber-like polymers based on chain statistics. Int J Solids Struct 43: 2–26.
  • Böl M, Sturmat M, Weichert C, Kober C. 2011. A new approach for the validation of skeletal muscle modelling using MRI data. Comput Mech 47: 591–601.
  • Boller M, Blaser S. 1998. Particles under stress. Water Sci Technol 37: 9–29.
  • Bott TR. 1998. Techniques for reducing the amount of biocide necessary to counteract the effects of biofilm growth in cooling water systems. Appl Therm Eng 18: 1059–1066.
  • Branda SS, Vik S, Friedman L, Kolter R. 2005. Biofilms: the matrix revisited. Trends Microbiol 13: 20–26.
  • Bremer PJ, Geese GG, Drake B. 1992. Atomic force microscopy examination of the topography of a hydrated bacterial biofilm on a copper surface. Curr Microbiol 24: 223–230.
  • Bundy KJ, Harris LG, Rahn BA, Richards RG. 2001. Measurement of fibroblast and bacterial detachment from biomaterials using jet impingement. Cell Biol Int 25: 289–307.
  • Busscher HJ, Weerkamp AH. 1987. Specific and non-specific interactions in bacterial adhesion to solid substrata. FEMS Microbiol Lett 46: 165–173.
  • Butt HJ, Cappella B, Kappl M. 2005. Force measurements with the atomic force microscope: technique, interpretation and applications. Surf Sci Rep 59: 1–152.
  • Cappella B, Dietler G. 1999. Force-distance curves by atomic force microscopy. Surf Sci Rep 34: 1–104.
  • Cense AW, Peeters EA, Gottenbos B, Baaijens FP, Nuijs AM, van Dongen ME. 2006. Mechanical properties and failure of Streptococcus mutans biofilms, studied using a microindentation device. J Microbiol Methods 67: 463–472.
  • Characklis WG. 1980. Biofilm development and destruction: Final Report, EPRI CS-1554, Project RP902-1. Electric Power Research Institute, Palo Alto, CA.
  • Characklis WG, Marshall KC. 1990. Biofilms: A basis for an interdisciplinary approach.. In: Characklis WG, Marshall KC. eds. Biofilms. New York: John Wiley & Sons, Inc..
  • Chaudhry MAS, Beg SA. 1998. A review on the mathematical modeling of biofilm processes: Advances in fundamentals of biofilm modeling. Chem Eng Tech 21, 701–710.
  • Chen MJ, Zhang Z, Bott TR. 1998. Direct measurement of the adhesive strength of biofilms in pipes by micromanipulation. Biotechnol Tech, 12: 875–880.
  • Chen MJ, Zhang Z, Bott TR. 2005. Effects of operating conditions on the adhesive strength of Pseudomonas fluorescens biofilms in tubes. Colloids Surf B Biointerfaces 43: 61–71.
  • Cheong F, Duarte S, Lee SH, Grier D. 2009. Holographic microrheology of polysaccharides from Streptococcus mutans biofilms. Rheol Acta 48: 109–115.
  • Chew JYM, Cardoso SSS, Paterson WR, Wilson DI. 2004a. CFD studies of dynamic gauging. Chem Eng Sci 59: 3381–3398.
  • Chew JYM, Paterson WR, Wilson DI. 2004b. Fluid dynamic gauging for measuring the strength of soft deposits. J Food Eng 65: 175–187.
  • Cogan NG. 2008. Two-fluid model of biofilm disinfection. Bull Math Biol 70: 800–819.
  • Cogan NG, Keener JP. 2004. The role of the biofilm matrix in structural development. Math Med Biol 21: 147–166.
  • Coman DR. 1944. Decreased mutual adhesiveness, a property of cells from squamous cell carcinomas. Cancer Res 4: 625–629.
  • Costerton JW. 1995. Overview of microbial biofilms. J Ind Microbiol 15: 137–140.
  • Costerton JW. 2007. The biofilm primer. Berlin, New York: Springer.
  • Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995. Microbial biofilms. Annu Rev Microbiol 49: 711–745.
  • Costerton JW, Montanaro L, Arciola CR. 2005. Biofilm in implant infections: its production and regulation. Int J Artif Organs 28: 1062–1068.
  • Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284: 1318–1322.
  • Coufort C, Derlon N, Ochoa-Chaves J, Liné A, Paul E. 2007. Cohesion and detachment in biofilm systems for different electron acceptor and donors. Water Sci Technol 55: 421–428.
  • Darouiche RO. 2004. Treatment of infections associated with surgical implants. N Engl J Med 350: 1422–1429.
  • Demirci A, Pometto AL 3rd, Ho KL. 1997. Ethanol production by Saccharomyces cerevisiae in biofilm reactors. J Ind Microbiol Biotechnol 19: 299–304.
  • Derlon N, Massé A, Escudié R, Bernet N, Paul E. 2008. Stratification in the cohesion of biofilms grown under various environmental conditions. Water Res 42: 2102–2110.
  • Deshpande MD, Vaishnav RN. 1982. Submerged laminar jet impingement on a plane. J Fluid Mech 114: 213–236.
  • Deshpande MD, Vaishnav RN. 1983. Wall stress distribution due to jet impingement. J Eng Mech-ASCE 109: 479–493.
  • Deshusses MA. 1997. Biological waste air treatment in biofilters. Curr Opin Biotechnol 8: 335–339.
  • Dockery J, Klapper I. 2001. Finger formation in biofilm layers. SIAM J Appl Math 62: 853–869.
  • Dohnt K, Sauer M, Müller M, Atallah K, Weidemann M, Gronemeyer P, Rasch D, Tielen P, Krull R. 2011. An in vitro urinary tract catheter system to investigate biofilm development in catheter-associated urinary tract infections. J Microbiol Methods 87: 302–308.
  • Donlan RM. 2002. Biofilms: microbial life on surfaces. Emerging Infect Dis 8: 881–890.
  • Dufrêne YF. 2008. Towards nanomicrobiology using atomic force microscopy. Nat Rev Microbiol 6: 674–680.
  • Dunsmore BC, Jacobsen A, Hall-Stoodley L, Bass CJ, Lappin-Scott HM, Stoodley P. 2002. The influence of fluid shear on the structure and material properties of sulphate-reducing bacterial biofilms. J Ind Microbiol Biotechnol 29: 347–353.
  • Dupin HJ, Kitanidis PK, McCarty PL. 2001. Pore-scale modeling of biological clogging due to aggregate expansion: A material mechanics approach. Water Resour Res 37: 2965–2979.
  • Dupres V, Alsteens D, Andre G, Dufrêne YF. 2010. Microbial nanoscopy: a closer look at microbial cell surfaces. Trends Microbiol 18: 397–405.
  • Dürr S, Thomason J. 2009. Biofouling. John Wiley & Sons.
  • Eberl H, Morgenroth E, Noguera D, Picioreanu C, Rittmann B, van Loosdrecht M, Wanner O. 2006. Mathematical modeling of biofilms. volume 18 of Scientific and Technical Report. London, UK: IWA Publishing.
  • Emerson RJ 4th, Camesano TA. 2004. Nanoscale investigation of pathogenic microbial adhesion to a biomaterial. Appl Environ Microbiol 70: 6012–6022.
  • Fang HH, Chan KY, Xu LC. 2000. Quantification of bacterial adhesion forces using atomic force microscopy (AFM). J Microbiol Methods 40: 89–97.
  • Fernández P, Heymann L, Ott A, Aksel N, Pullarkat PA. 2007.Shear rheology of a cell monolayer. New J Phys 9: 419.
  • Ferry JD. 1980. Viscoelastic properties of polymers., 3rd ed.New York: Wiley.
  • Findley WN, Lai JS, Onaran K. 1989. Creep and relaxation of nonlinear viscoelastic materials: With an introduction to linear viscoelasticity. Mineola, NY: Dover.
  • Flemming HC. 1997. Reverse osmosis membrane biofouling. Exp Therm Fluid Sci 14: 382–391.
  • Fukaya M, Park YS, Toda K. 1992. Improvement of acetic acid fermentation by molecular breeding and process development. J Appl Microbiol 73: 447–454.
  • Fung YC. 1993. Biomechanics: Mechanical properties of living tissues., 2nd ed. Berlin and New York: Springer-Verlag.
  • Gross R, Lang K, Bühler K, Schmid A. 2010. Characterization of a biofilm membrane reactor and its prospects for fine chemical synthesis. Biotechnol Bioeng 105: 705–717.
  • Guélon T, Mathias JD, Stoodley P. 2011. Advances in biofilm mechanics. In: Flemming HC, Wingender I, Szewzyk U, ed. Biofilm Highlights. Berlin, Heidelberg: Springer, 111–139.
  • Habash M, Reid G. 1999. Microbial biofilms: their development and significance for medical device-related infections. J Clin Pharmacol 39: 887–898.
  • Hadi R, Vickery K, Deva A, Charlton T. 2010. Biofilm removal by medical device cleaners: comparison of two bioreactor detection assays. J Hosp Infect 74: 160–167.
  • Haupt P. 2002. Continuum mechanics and theory of materials., 2nd ed. Berlin, New York: Springer.
  • Hempel DC, Krull R. 1996. Biologische Behandlung von Abwässern mit schwer abbaubaren Inhaltsstoffen. In: Brauer H, ed. Handbuch des Umweltschutzes und der Umweltschutztechnik: Bd 4: Additiver Umweltschutz: Behandlung von Abwässern. Berlin, Heidelberg: Springer Verlag, 321–390.
  • Hertz H. 1882. Über die Berührung fester elastischer Körper. J Reine Angew Math 92: 156–171.
  • Herzberg M, Elimelech M. 2007. Biofouling of reverse osmosis membranes: Role of biofilm-enhanced osmotic pressure. J Membrane Sci 295: 11–20.
  • Hill R. 1968. On constitutive inequalities for simple materials - I. J Mech Phys Solids 16: 229–242.
  • Hohne DN, Younger JG, Solomon MJ. 2009. Flexible microfluidic device for mechanical property characterization of soft viscoelastic solids such as bacterial biofilms. Langmuir 25: 7743–7751.
  • Holzapfel GA. 2000. Nonlinear solid mechanics: A continuum approach for engineering. Chichester: John Wiley & Sons.
  • Hooper RJ, Liu W, Fryer PJ, Paterson WR, Wilson DI, Zhang Z. 2006. Comparative studies of fluid dynamic gauging and a micromanipulation probe for strength measurements. Food Bioprod Process 84: 353–358.
  • Houari A, Picard J, Habarou H, Galas L, Vaudry H, Heim V, Di Martino P. 2008. Rheology of biofilms formed at the surface of NF membranes in a drinking water production unit. Biofouling 24: 235–240.
  • Jarvis P, Jefferson B, Gregory J, Parsons SA. 2005. A review of floc strength and breakage. Water Res 39: 3121–3137.
  • Johnson KL. 2004. Contact mechanics. Cambridge: Cambridge Univ. Press.
  • Klapper I. 2004. Effect of heterogeneous structure in mechanically unstressed biofilms on overall growth. Bull Math Biol 66: 809–824.
  • Klapper I, Dockery J. 2006. Role of cohesion in the material description of biofilms. Phys Rev E 74: 031902.
  • Klapper I, Rupp CJ, Cargo R, Purvedorj B, Stoodley P. 2002. Viscoelastic fluid description of bacterial biofilm material properties. Biotechnol Bioeng 80: 289–296.
  • Korber DR, James GA, Costerton JW. 1994a. Evaluation of fleroxacin activity against established Pseudomonas fluorescens biofilms. Appl Environ Microbiol 60: 1663–1669.
  • Korber DR, Lawrence JR, Caldwell DE. 1994b. Effect of motility on surface colonization and reproductive success of Pseudomonas fluorescens in dual-dilution continuous culture and batch culture systems. Appl Environ Microbiol 60: 1421–1429.
  • Körstgens V. 2003. Die mechanische Stabilität bakterieller Biofilme - eine Untersuchung verschiedener Einflüsse auf Biofilme von Pseudomonas aeruginosa. Ph.D. thesis; Universität Duisburg-Essen, Fakultät für Naturwissenschaften.
  • Körstgens V, Flemming HC, Wingender J, Borchard W. 2001a. Uniaxial compression measurement device for investigation of the mechanical stability of biofilms. J Microbiol Methods 46: 9–17.
  • Körstgens V, Flemming HC, Wingender J, Borchard W. 2001b. Influence of calcium ions on the mechanical properties of a model biofilm of mucoid Pseudomonas aeruginosa. Water Sci Technol 43: 49–57.
  • Koza A, Hallett PD, Moon CD, Spiers AJ. 2009. Characterization of a novel air-liquid interface biofilm of Pseudomonas fluorescens SBW25. Microbiology 155: 1397–1406.
  • Kreth J, Hagerman E, Tam K, Merritt J, Wong DT, Wu BM, Myung NV, Shi W, Qi F. 2004. Quantitative analyses of Streptococcus mutans biofilms with quartz crystal microbalance, microjet impingement and confocal microscopy. Biofilms 1: 277–284.
  • Kumar CG, Anand SK. 1998. Significance of microbial biofilms in food industry: a review. Int J Food Microbiol 42: 9–27.
  • Lahaye E, Aubry T, Kervarec N, Douzenel P, Sire O. 2007a. Does water activity rule P. mirabilis periodic swarming? I. Biochemical and functional properties of the extracellular matrix. Biomacromolecules 8: 1218–1227.
  • Lahaye E, Aubry T, Fleury V, Sire O. 2007b. Does water activity rule P. mirabilis periodic swarming? II. Viscoelasticity and water balance during swarming. Biomacromolecules 8: 1228–1235.
  • Lakes RS. 1999. Viscoelastic solids. CRC Mechanical Engineering Series, Vol 9. Boca Raton: CRC Press.
  • Lappin-Scott HM, Costerton JW. 1995. Microbial biofilms., 1st ed. Cambridge, New York: Cambridge University Press.
  • Laspidou CS, Kungolos A, Samaras P. 2010. Cellular-automata and individual-based approaches for the modeling of biofilm structures: Pros and cons. Desalination 250: 390–394.
  • Lau PC, Dutcher JR, Beveridge TJ, Lam JS. 2009a. Absolute quantitation of bacterial biofilm adhesion and viscoelasticity by microbead force spectroscopy. Biophys J 96: 2935–2948.
  • Lau PC, Lindhout T, Beveridge TJ, Dutcher JR, Lam JS. 2009b. Differential lipopolysaccharide core capping leads to quantitative and correlated modifications of mechanical and structural properties in Pseudomonas aeruginosa biofilms. J Bacteriol 191: 6618–6631.
  • Lawrence JR, Neu TR. 2003. Microscale analyses of the formation and nature of microbial biofilm communities in river systems. Rev Environ Sci Biotechnol 2: 85–97.
  • Lazarova V, Manem J. 1995. Biofilm characterization and activity analysis in water and wastewater treatment. Water Res 29: 2227–2245.
  • LeChevallier MW, Babcock TM, Lee RG. 1987. Examination and characterization of distribution system biofilms. Appl Environ Microbiol 53: 2714–2724.
  • Lee SH, Grier DG. 2007. Holographic microscopy of holographically trapped three-dimensional structures. Opt Express 15: 1505–1512.
  • Lens P, Moran AP, Mahony T, Stoodley P, O’Flaherty V. 2003. Biofilms in medicine, industry and environmental biotechnology: Characteristics, analysis and control. London: IWA Publishing.
  • Liu W, Christian GK, Zhang Z, Fryer PJ. 2002. Development and use of a micromanipulation technique for measuring the force required to disrupt and remove fouling deposits: Fouling, Cleaning and Disinfection. Food Bioprod Process 80: 286–291.
  • Liu W, Christian GK, Zhang Z, Fryer PJ. 2006. Direct measurement of the force required to disrupt and remove fouling deposits of whey protein concentrate. Int Dairy J 16: 164–172.
  • Ludensky M. 2003. Control and monitoring of biofilms in industrial applications. Int Biodeter Biodegr 51: 255–263.
  • Macfarlane S, McBain AJ, Macfarlane GT. 1997. Consequences of biofilm and sessile growth in the large intestine. Adv Dent Res 11: 59–68.
  • MacKintosh FC, Schmidt CF. 1999. Microrheology. Curr Opin Colloid In 4: 300–307.
  • Macosko CW. 1994. Rheology: Principles, measurements, and applications. New York : VCH.
  • Martins dos Santos VAP, Yakimov MM, Timmis KN, Golyshin PN. 2008. Genomic insights into oil biodegradation in marine systems.. In: Díaz E, ed. Microbial Biodegradation: Genomics and Molecular Biology. Norfolk, UK: Caister Academic Press, 269–296.
  • Mason TG, Ganesan K, van Zanten JH, Wirtz D, Kuo SC. 1997. Particle tracking microrheology of complex fluids. Phys Rev Lett 79: 3282–3285.
  • Mathias JD, Stoodley P. 2009. Applying the digital image correlation method to estimate the mechanical properties of bacterial biofilms subjected to a wall shear stress. Biofouling 25: 695–703.
  • Miehe C, Göktepe S, Lulei F. 2004. A micro-macro approach to rubber-like materials - Part I: the non-affine micro-sphere model of rubber elasticity. J Mech Phys Solids 52: 2617–2660.
  • Möhle RB, Langemann T, Haesner M, Augustin W, Scholl S, Neu TR, Hempel DC, Horn H. 2007. Structure and shear strength of microbial biofilms as determined with confocal laser scanning microscopy and fluid dynamic gauging using a novel rotating disc biofilm reactor. Biotechnol Bioeng 98: 747–755.
  • Moresi M, Bruno M, Parente E. 2004. Viscoelastic properties of microbial alginate gels by oscillatory dynamic tests. J Food Eng 64: 179–186.
  • Morikawa M. 2006. Beneficial biofilm formation by industrial bacteria Bacillus subtilis and related species. J Biosci Bioeng 101: 1–8.
  • Müller DJ, Dufrêne YF. 2008. Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology. Nat Nanotechnol 3: 261–269.
  • Müller DJ, Helenius J, Alsteens D, Dufrêne YF. 2009. Force probing surfaces of living cells to molecular resolution. Nat Chem Biol 5: 383–390.
  • Nadell CD, Xavier JB, Foster KR. 2009. The sociobiology of biofilms. FEMS Microbiol Rev 33: 206–224.
  • Neu TR. 1996. Significance of bacterial surface-active compounds in interaction of bacteria with interfaces. Microbiol Rev 60: 151–166.
  • Nicolella C, van Loosdrecht MC, Heijnen JJ. 2000. Wastewater treatment with particulate biofilm reactors. J Biotechnol 80: 1–33.
  • Norris CH. 1939. The tension at the surface, and other physical properties of the nucleated erythrocyte. J Cell Compar Physl 14: 117–133.
  • Ochoa JC, Coufort C, Escudié R, Liné A, Paul E. 2007. Influence of non-uniform distribution of shear stress on aerobic biofilms. Chem Eng Sci 62: 3672–3684.
  • Oh YJ, Jo W, Yang Y, Park S. 2007. Influence of culture conditions on Escherichia coli O157:H7 biofilm formation by atomic force microscopy. Ultramicroscopy 107: 869–874.
  • Oh YJ, Lee NR, Jo W, Jung WK, Lim JS. 2009. Effects of substrates on biofilm formation observed by atomic force microscopy. Ultramicroscopy 109: 874–880.
  • Ohashi A, Harada H. 1994a, Adhesion strength of biofilm developed in an attached- growth reactor. Water Sci Technol 29: 281–288.
  • Ohashi A, Harada H. 1994b. Characterization of detachment mode of biofilm developed in an attached-growth reactor. Water Sci Technol 30: 35–45.
  • Ohashi A, Harada H. 1996. A novel concept for evaluation of biofilm adhesion strength by applying tensile force and shear force. Water Sci Technol 34: 201–211.
  • Ohashi A, Koyama T, Syutsubo K, Harada H. 1999. A novel method for evaluation of biofilm tensile strength resisting erosion. Water Sci Technol 39: 261–268.
  • Ohashi T, Ishii Y, Ishikawa Y, Matsumoto T, Sato M. 2002. Experimental and numerical analyses of local mechanical properties measured by atomic force microscopy for sheared endothelial cells. Biomed Mater Eng 12: 319–327.
  • Otto K. 2008. Biophysical approaches to study the dynamic process of bacterial adhesion. Res Microbiol 159: 415–422.
  • Paramonova E, Kalmykowa OJ, van der Mei HC, Busscher HJ, Sharma PK. 2009a. Impact of hydrodynamics on oral biofilm strength. J Dent Res 88: 922–926.
  • Paramonova E, Krom BP, van der Mei HC, Busscher HJ, Sharma PK. 2009b. Hyphal content determines the compression strength of Candida albicans biofilms. Microbiology 155: 1997–2003.
  • Picioreanu C, van Loosdrecht MCM. 2003. Use of mathematical modelling to study biofilm development and morphology.. In: Biofilms in Medicine, Industry and Environmental Biotechnology: Characteristics, Analysis and Control. IWA Publishing, 413–437.
  • Picioreanu C, van Loosdrecht MC, Heijnen JJ. 2001. Two-dimensional model of biofilm detachment caused by internal stress from liquid flow. Biotechnol Bioeng 72: 205–218.
  • Picioreanu C, Xavier JB, van Loosdrecht MCM. 2004. Advances in mathematical modeling of biofilm structure. Biofilms 1: 337–349.
  • Poppele EH. 2006. The Cohesive Strength of Biofilms. Ph.D. thesis, University of Minnesota.
  • Poppele EH, Hozalski RM. 2003. Micro-cantilever method for measuring the tensile strength of biofilms and microbial flocs. J Microbiol Methods 55: 607–615.
  • Potera C. 1996. Biofilms invade microbiology. Science 273: 1795–1797.
  • Radmacher M, Tillmann RW, Fritz M, Gaub HE. 1992. From molecules to cells: imaging soft samples with the atomic force microscope. Science 257: 1900–1905.
  • Rodriguez A, Autio WR, McLandsborough LA. 2008. Effects of contact time, pressure, percent relative humidity (%RH), and material type on Listeria biofilm adhesive strength at a cellular level using atomic force microscopy (AFM). Food Biophys 3: 305–311.
  • Rogers SS, van der Walle C, Waigh TA. 2008. Microrheology of bacterial biofilms in vitro: Staphylococcus aureus and Pseudomonas aeruginosa. Langmuir 24: 13549–13555.
  • Rubinstein M, Colby RH. 2006. Polymer physics. Reprint. ed. New York: Oxford University Press.
  • Rupp CJ, Fux CA, Stoodley P. 2005. Viscoelasticity of Staphylococcus aureus biofilms in response to fluid shear allows resistance to detachment and facilitates rolling migration. Appl Environ Microbiol 71: 2175–2178.
  • Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184: 1140–1154.
  • Savin T, Doyle PS. 2005. Static and dynamic errors in particle tracking microrheology. Biophys J 88: 623–638.
  • Schachter B. 2003. Slimy business–the biotechnology of biofilms. Nat Biotechnol 21: 361–365.
  • Schooling SR, Beveridge TJ. 2006. Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188: 5945–5957.
  • Schultz MP, Swain GW. 2000. The influence of biofilms on skin friction drag. Biofouling 15: 129–139.
  • Seth BR. 1964. Generalized strain measures with application to physical problems.. In: Reiner M, Abir D. eds. Second-order effects in elasticity, plasticity and fluid dynamics. New York: Pergamon Press, 162–172.
  • Shaw T, Winston M, Rupp CJ, Klapper I, Stoodley P. 2004. Commonality of elastic relaxation times in biofilms. Phys Rev Lett 93: 098102.
  • Sheng J, Malkiel E, Katz J. 2006. Digital holographic microscope for measuring three-dimensional particle distributions and motions. Appl Opt 45: 3893–3901.
  • Sheng X, Ting YP, Pehkonen SO. 2007. Force measurements of bacterial adhesion on metals using a cell probe atomic force microscope. J Colloid Interface Sci 310: 661–669.
  • Shukla A, Fuchs R, Rehage H. 2006. Quasi-anomalous diffusion processes in entangled solutions of wormlike surfactant micelles. Langmuir 22: 3000–3006.
  • Shunmugaperumal T. 2010. Biofilm eradication and prevention: A pharmaceutical approach to medical device infections. Hoboken, N.J: Wiley.
  • Sichel FJM. 1934. The elasticity of isolated resting skeletal muscle fibres. J Cell and Compar Physl 5: 21–42.
  • Solomon MJ, Lu Q. 2001. Rheology and dynamics of particles in viscoelastic media. Curr Opin Colloid In 6: 430–437.
  • Spiers AJ, Bohannon J, Gehrig SM, Rainey PB. 2003. Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 50: 15–27.
  • Srivastava RB, Awasthi M, Upreti MC, Mathur GN. 2006. Studies on Aureobasidium pullulans forming biofilm on high strength aluminium alloy, a structural component, in aircraft fuel tanks. Indian J Eng Mater S 13: 135–139.
  • Steele A, Goddard DT, Beech IB. 1994. An atomic force microscopy study of the biodeterioration of stainless steel in the presence of bacterial biofilms. Int Biodeter Biodegr 34: 35–46.
  • Stickler DJ. 1996. Bacterial biofilms and the encrustation of urethral catheters. Biofouling 9: 293–305
  • Stoodley P, Cargo R, Rupp CJ, Wilson S, Klapper I. 2002a. Biofilm material properties as related to shear-induced deformation and detachment phenomena. J Ind Microbiol Biotechnol 29: 361–367.
  • Stoodley P, Dodds I, Boyle JD, Lappin-Scott HM. 1998a. Influence of hydrodynamics and nutrients on biofilm structure. J Appl Microbiol 85 Suppl 1: 19S–28S.
  • Stoodley P, Jacobsen A, Dunsmore BC, Purevdorj B, Wilson S, Lappin-Scott HM, Costerton JW. 2001. The influence of fluid shear and AICI3 on the material properties of Pseudomonas aeruginosa PAO1 and Desulfovibrio sp. EX265 biofilms. Water Sci Technol 43: 113–120.
  • Stoodley P, Lewandowski Z, Boyle JD, Lappin-Scott HM. 1998b. Oscillation characteristics of biofilm streamers in turbulent flowing water as related to drag and pressure drop. Biotechnol Bioeng 57: 536–544.
  • Stoodley P, Lewandowski Z, Boyle JD, Lappin-Scott HM. 1999. Structural deformation of bacterial biofilms caused by short-term fluctuations in fluid shear: an in situ investigation of biofilm rheology. Biotechnol Bioeng 65: 83–92.
  • Stoodley P, Sauer K, Davies DG, Costerton JW. 2002b. Biofilms as complex differentiated communities. Annu Rev Microbiol 56: 187–209.
  • Taherzadeh D, Picioreanu C, Küttler U, Simone A, Wall WA, Horn H. 2010. Computational study of the drag and oscillatory movement of biofilm streamers in fast flows. Biotechnol Bioeng 105: 600–610.
  • Talvy S, Ochoa J, Paul E, Liné A. 2011. Influence of the nature of hydrodynamic constraints on aerobic biofilms. Int J Environ Waste M 7: 4–23.
  • te Nijenhuis K, McKinley GH, Spiegelberg SF, Barnes HA, Aksel N, Heymann L, Odell JA. 2007. Non-Newtonian Flows.. In: Tropea C, Yarin AL, Foss IF. eds. Springer handbook of experimental fluid mechanics. Berlin, Heidelberg: Springer, 619–744.
  • Teixeira AV, Geissler E, Licinio P. 2007. Dynamic scaling of polymer gels comprising nanoparticles. J Phys Chem B 111: 340–344.
  • Thomas CR, Zhang Z, Cowen C. 2000. Micromanipulation measurements of biological materials. Biotechnol Lett 22: 531–537.
  • Thomas JG, Litton I, Rinde H. 2005. Economic impact of biofilms on treatment costs. In: Pace JL, Rupp ME, Finch RG . eds. Biofilms, infection, and antimicrobial therapy. Boca Raton, FL: Taylor & Francis, 21–38.
  • Towler BW, Cunningham A, Stoodley P, McKittrick L. 2007. A model of fluid-biofilm interaction using a Burger material law. Biotechnol Bioeng 96: 259–271.
  • Towler BW, Rupp CJ, Cunningham AB, Stoodley P. 2003. Viscoelastic properties of a mixed culture biofilm from rheometer creep analysis. Biofouling 19: 279–285.
  • Townsin RL. 2003. The ship hull fouling penalty. Biofouling 19 Suppl: 9–15.
  • Truesdell C, Noll W. 1992. The non-linear field theories of mechanics., 2nd ed. Berlin and Heidelberg: Springer-Verlag.
  • Tuladhar TR, Paterson WR, Macleod N, Wilson DI. 2000. Development of a novel non-contact proximity gauge for thickness measurement of soft deposits and its application in fouling studies. Can J Chem Eng 78: 935–947.
  • Vaishnav RN, Patel DJ, Atabek HB. 1978. Properties of intimal layer and adjacent flow. J Eng Mech Div 104: 67–77.
  • Vaishnav RN, Patel DJ, Atabek HB, Deshpande MD, Plowman F, Vossoughi J. 1983. Determination of the local erosion stress of the canine endothelium using a jet impingement method. J Biomech Eng 105: 77–83.
  • Vieira MJ, Melo LF, Pinheiro MM. 1993. Biofilm formation: Hydrodynamic effects on internal diffusion and structure. Biofouling 7: 67–80.
  • Vinogradov AM, Winston M, Rupp CJ, Stoodley P. 2004. Rheology of biofilms formed from the dental plaque pathogen Streptococcus mutans. Biofilms 1: 49–56.
  • van Loosdrecht MC, Heijnen JJ, Eberl H, Kreft J, Picioreanu C. 2002. Mathematical modelling of biofilm structures. Antonie Van Leeuwenhoek 81: 245–256.
  • Volle CB, Ferguson MA, Aidala KE, Spain EM, Núñez ME. 2008. Spring constants and adhesive properties of native bacterial biofilm cells measured by atomic force microscopy. Colloids Surf B Biointerfaces 67: 32–40.
  • Waigh TA. 2005. Microrheology of complex fluids. Rep Prog Phys 68: 685–742.
  • Wang Q, Zhang T. 2010. Review of mathematical models for biofilms. Solid State Commun 150: 1009–1022.
  • Webb HK, Truong VK, Hasan J, Crawford RJ, Ivanova EP. 2011. Physico-mechanical characterisation of cells using atomic force microscopy - Current research and methodologies. J Microbiol Methods 86: 131–139.
  • Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.
  • Wilking JN, Angelini TE, Seminara A, Brenner MP, Weitz DA. 2011. Biofilms as complex fluids. MRS Bull 36: 385–391.
  • Wilson M. 2001. Bacterial biofilms and human disease. Sci Prog 84: 235–254.
  • Wimpenny JW. 2000. An overview of biofilms as functional communities. In: Allison DG, Gilbert P, Lappin-Scott HM, Wilson M. eds. Community structure and co-operation in biofilms. Cambridge, UK: Cambridge University Press, 1–24.
  • Wimpenny JW, Colasanti R. 1997. A unifying hypothesis for the structure of microbial biofilms based on cellular automaton models. FEMS Microbiol Ecol 22: 1–16.
  • Wirtz D. 2009. Particle-tracking microrheology of living cells: principles and applications. Annu Rev Biophys 38: 301–326.
  • Wloka M, Rehage H, Flemming HC, Wingender J. 2004. Rheological properties of viscoelastic biofilm extracellular polymeric substances and comparison to the behavior of calcium alginate gels. Colloid Polym Sci 282: 1067–1076.
  • Wloka M, Rehage H, Flemming HC, Wingender J. 2005. Structure and rheological behaviour of the extracellular polymeric substance network of mucoid Pseudomonas aeruginosa biofilms. Method Enzymol 2: 275–283.
  • Wright CJ, Shah MK, Powell LC, Armstrong I. 2010. Application of AFM from microbial cell to biofilm. Scanning 32: 134–149.
  • Xu J, Viasnoff V, Wirtz D. 1998. Compliance of actin filament networks measured by particle-tracking microrheology and diffusing wave spectroscopy. Rheol Acta 37: 387–398.
  • Yeung A, Gibbs A, Pelton R. 1997. Effect of shear on the strength of polymer-induced flocs. J Colloid Interface Sci 196: 113–115.
  • Yeung AKC, Pelton R. 1996. Micromechanics: A new approach to studying the atrength and breakup of flocs. J Colloid Interface Sci 184: 579–585.
  • Zhang T, Cogan NG, Wang Q. 2008a. Phase-field models for biofilms. I. Theory and one-dimensional simulations. SIAM J Appl Math 69: 641–669.
  • Zhang T, Cogan N, Wang Q. 2008b. Phase-field models for biofilms II. 2-D numerical simulations of biofilm-flow interaction. Commun Comput Phys 4: 72–101.
  • Zhang Z, Ferenczi MA, Lush AC, Thomas CR. 1991. A novel micromanipulation technique for measuring the bursting strength of single mammalian cells. Appl Microbiol Biotechnol 36: 208–210.
  • Zhang Z, Ferenczi MA, Thomas CR. 1992. A micromanipulation technique with a theoretical cell model for determining mechanical properties of single mammalian cells. Chem Eng Sci 47: 1347–1354.
  • Zhang Z, Sisk ML, Mashmoushy H, Thomas CR. 1999. Characterisation of the breaking force of latex particle aggregates by micromanipulation. Part Part Syst Char 16: 278–283.
  • Žagar G, Onck PR, van der Giessen E. 2011. Elasticity of rigidly cross-linked networks of athermal filaments. Macromolecules 44: 7026–7033.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.