Skip to main content

Advertisement

SpringerLink
Log in

Effect of inertial acoustic cavitation on antibiotic efficacy in biofilms

  • Published:
Applied Mathematics and Mechanics Aims and scope Submit manuscript

Abstract

Bacterial biofilms can lead to chronic infections, increase tolerance to antibiotics and disinfectants, resistance to phagocytosis, and other components of the body’s immune system. Biofilm formation is implicated in the persistence of staphylococcal infections and chronic Pseudomonas aeruginosa lung infections in cystic fibrosis (CF) patients (which can result from biofilm-growing mucoid strains). Conventional treatments utilize aggressive antibiotic prophylaxis/therapy to prevent/eliminate biofilms, followed by chronic suppressive therapy. Recently, the use of enzymes to dissolve the biofilm matrix was investigated, in addition to quorum sensing inhibitors to increase biofilm susceptibility to antibiotics. Here, we propose a novel strategy, utilizing ultrasound-induced inertial cavitation, to increase antibiotic efficacy. The wall shear stress at the biofilm interface is calculated, and viscoplastic constitutive equations are used to examine the biofilm response to the mechanical stress. Our simulations suggest that the maximum biofilm detachment occurs at high pressure/low frequency, and the mechanical disruption can affect the biochemical processes inside the biofilm resulting in vulnerability to antibiotics.

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

Similar content being viewed by others

References

  1. HALL-STOODLEY, L., COSTERTON, J. W., and STOODLEY, P. Bacterial biofilms: from the natural environment to infectious diseases. Nature Reviews Microbiology, 2(2), 95–108 (2004)

    Article  Google Scholar 

  2. IMRAN, M. and SMITH, H. A model of optimal dosing of antibiotic treatment in biofilm. Mathematical Biosciences and Engineering, 11(3), 547–571 (2014)

    Article  MathSciNet  MATH  Google Scholar 

  3. WU, H., MOSER, C., WANG, H. Z., HØIBY, N., and SONG, Z. J. Strategies for combating bacterial biofilm infections. International Journal of Oral Science, 7, 1–7 (2015)

    Article  Google Scholar 

  4. ANDERL, J. N., FRANKLIN, M. J., and STEWART, P. S. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrobial Agents Chemother, 4(7), 1818–1824 (2000)

    Article  Google Scholar 

  5. CHAMBLESS, J. D., HUNT, S. M., and STEWART, P. S. A three-dimensional computer model of four hypothetical mechanisms protecting biofilms from antimicrobials. Applied and Environmental Microbiology Journal, 72(3), 2005–2013 (2006)

    Article  Google Scholar 

  6. MAH, T. C. and O’TOOLE, G. A. Mechanisms of biofilm resistance to antimicrobial agents. Trends in Microbiology, 9(1), 34–39 (2001)

    Article  Google Scholar 

  7. POULSEN, L. V. Microbial biofilm in food processing. LWT-Food Science and Technology, 32(6), 321–326 (1999)

    Article  Google Scholar 

  8. STEWART, P. S. and COSTERTON, J. E. Antibiotic resistance of bacteria in biofilms. Lancet, 358, 135–38 (2001)

    Article  Google Scholar 

  9. ANDERSEN, P. C., BRODBECK, B. V., ODEN, S., SHRINER, A., and LEITE, B. Influence of xylem fluid chemistry on planktonic growth, biofilm formation and aggregation of xylella fastidiosa. FEMS Microbiology Letters, 274(2), 210–217 (2007)

    Article  Google Scholar 

  10. BJARNSHOLT, T. The role of bacterial biofilms in chronic infections. APMIS, 121(s136), 1–58 (2013)

    Article  Google Scholar 

  11. VEERACHAMY, S., YARLAGADDA, T., MANIVASAGAM, G., and YARLAGADDA, P. K. Bacterial adherence and biofilm formation on medical implants: a review. Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine, 228, 1083–1099 (2014)

    Article  Google Scholar 

  12. GUPTA, P., SARKAR, S., DAS, B., BHATTACHARJEE, S., and TRIBEDI, P. Biofilm, pathogenesis and prevention—a journey to break the wall: a review. Arch Microbiol, 198, 1–15 (2016)

    Article  Google Scholar 

  13. PERCIVAL, S. L., SULEMAN, L., VUOTTO, C., and DONELLI, G. Healthcare-associated infections, medical devices and biofilms: risk, tolerance and control. Journal of Medical Microbiol, 64, 323–334 (2015)

    Article  Google Scholar 

  14. PICIOREANU, C., VAN LOOSDRECHT, M. C. M., and HEIJNEN, J. J. Two-dimensional model of biofilm detachment caused by internal stress from liquid flow. Biotechnology and Bioengineering, 72(2), 205–218 (2001)

    Article  Google Scholar 

  15. IQBAL, K., OHL, S. W., KHOO, B. C., NEO, J., FAWZY, A. S., and AMR, S. Effect of high-intensity focused ultrasound on enterococcus faecalis planktonic suspensions and biofilms. Ultrasound in Medicine and Biology, 39(5), 825–833 (2013)

    Article  Google Scholar 

  16. KOO, H., ALLAN, R. N., HOWLIN, R. P., STOODLEY, P., and HALL-STOODLEY, L. Targeting microbial biofilms: current and prospective therapeutic strategies. Nature Reviews Microbiology, 15, 740 (2017)

    Article  Google Scholar 

  17. BRENNEN, C. E. Cavitation and Bubble Dynamics, Cambridge University Press, Cambridge (2013)

    Book  MATH  Google Scholar 

  18. PLESSET, M. S. and PROSPERETTI, A. Bubble dynamics and cavitation. Annual Review of Fluid Mechanics, 9, 145–185 (1977)

    Article  MATH  Google Scholar 

  19. LAUTERBORN, W. and METTIN, R. Acoustic cavitation: bubble dynamics in high power ultrasonic fields. Power Ultrasonics, 2015, 37–78 (2015)

    Article  Google Scholar 

  20. CHAHINE, G. L., KAPAHI, A., CHOI, J. K., and HSIAO, C. T. Modeling of surface cleaning by cavitation bubble dynamics and collapse. Ultrasonics Sonochemistry, 29, 528–549 (2016)

    Article  Google Scholar 

  21. FELVER, B., KING, D. C., LEA, S. C., PRICE, G. J., and WALMSLEY, A. D. Cavitation occurrence around ultrasonic dental scalers. Ultrasonics Sonochemistry, 16, 692–697 (2009)

    Article  Google Scholar 

  22. NAKAJIMA, K., NISHIOKA, D., HIRAO, M., SO, M., GOTO, Y., and OGI, H. Drastic acceleration of fibrillation of insulin by transient cavitation bubble. Ultrasonics Sonochemistry, 36, 206–211 (2017)

    Article  Google Scholar 

  23. OHL, C. D., ARORA, M., IKINK, R., DE-JONG, N., VERSLUIS, M., DELIUS, M, and LOHSE, M. Sonoporation from jetting cavitation bubbles. Biophysical Journal, 91, 4285–4295 (2006)

    Article  Google Scholar 

  24. PISHCHALNIKOV, Y. A., SAPOZHNIKOV, O. A., BAILEY, M. R., WILLIAMS, J. C., COLONIUS, T., CRUM, L. A., and EVAN, A. P. Cavitation bubble cluster activity in the breakage of kidney stones by lithotripter shockwaves. Journal of Endourology, 17, 435–446 (2003)

    Article  Google Scholar 

  25. ALPKVIST, E. and KLAPPER, I. Description of mechanical response including detachment using a novel particle model of biofilm/flow interaction. Water Science and Technology, 55(8–9), 265–273 (2007)

    Article  Google Scholar 

  26. COGAN, N. G., CORTEZ, R., and FAUCI, L. Modeling physiological resistance in bacterial biofilms. Bulletin of Mathematical Biology, 67(4), 831–853 (2005)

    Article  MathSciNet  MATH  Google Scholar 

  27. DUDDU, R., CHOPP, D. L., and MORAN, B. A two-dimensional continuum model of biofilm growth incorporating fluid flow and shear stress based detachment. Biotechnology and Bioengineering, 103(1), 92–104 (2009)

    Article  Google Scholar 

  28. EBERL, H. J. and SUDARSAN, R. Exposure of biofilms to slow flow fields: the convective contribution to growth and disinfection. Journal of Theoretical Biology, 253, 788–807 (2008)

    Article  MathSciNet  MATH  Google Scholar 

  29. GHASEMI, M., HENSE, B. A., EBERL, H. J., and KUTTLER, C. Simulation-based exploration of quorum sensing triggered resistance of biofilms to antibiotics. Bulletin of Mathematical Biology, 80, 1736–1775 (2018)

    Article  MathSciNet  MATH  Google Scholar 

  30. JAYATHILAKE, P. G., GUPTA, P., LI, B., MADSEN, C., OYEBAMIJI, O., and GONZALEZ-CABALEIRO, R. A mechanistic individual-based model of microbial communities. PLoS One, 12(8), e0181965 (2017)

    Article  Google Scholar 

  31. KLAPPER, I. and DOCKERY, J. Mathematical description of microbial biofilms. SIAM Review, 52(2), 221–265 (2010)

    Article  MathSciNet  MATH  Google Scholar 

  32. SEELUANGSAWAT, P. 3-D Computational Investigation of Viscoelastic Biofilms Using GPUs, Ph. D. dissertation, University of South Carolina, South Carolina (2011)

    Google Scholar 

  33. SMITH, B., VAUGHAN, B., and CHOPP, D. The extended finite element method for boundary layer problems in biofilm growth. Communications in Applied Mathematics and Computational Science, 2(1), 35–56 (2007)

    Article  MathSciNet  MATH  Google Scholar 

  34. SZOMOLAY, B., KLAPPER, I., and DINDOS, M. Analysis of adaptive response to dosing protocols for biofilm control. SIAM Journal on Applied Mathematics, 70, 3175–3202 (2010)

    Article  MathSciNet  MATH  Google Scholar 

  35. TAHERZADEH, D., PICIOREANU, C., and HORN, H. Mass transfer enhancement in moving biofilm structures. Biophysical Journal, 102(7), 1483–1492 (2012)

    Article  Google Scholar 

  36. VAN-LOOSDRECHT, M. C. M., HEIJNEN, J. J., EBERL, H., KREFT, J., and PICIOREANU, C. Mathematical modelling of biofilm structures. Antonie Van Leeuwenh, 81(1), 245–256 (2002)

    Article  Google Scholar 

  37. WANG, Q. and ZHANG, T. Review of mathematical models for biofilms. Solid State Communications, 150(21–22), 1009–1022 (2010)

    Article  Google Scholar 

  38. WANNER, O., EBERL, H. J., VAN LOOSDRECHT, M. C. M., MORGENROTH, E., NOGUERA, D. R., PICIOREANU, C., and RITTMANN, B. E. Mathematical Modelling of Biofilms, IWA Publishing, London (2006)

    Google Scholar 

  39. VERHAAGEN, B. and RIVAS, D. F. Measuring cavitation and its cleaning effect. Ultrasonics Sonochemistry, 29, 619–628 (2016)

    Article  Google Scholar 

  40. GUÉLON, T., MATHIAS, J. D., and STOODLEY P. Advances in Biofilm Mechanics, Springer, Berlin (2011)

    Book  Google Scholar 

  41. OHASHI, A. and HARADA, H. A novel concept for evaluation of biofilm adhesion strength by applying tensile force and shear force. Water Science and Technology, 34(5–6), 201–211 (1996)

    Article  Google Scholar 

  42. STOODLEY, P., CARGO, R., RUPP, C. J., WILSON, S., and KLAPPER, I. Biofilm material properties as related to shear-induced deformation and detachment phenomena. Journal of Industrial Microbiology and Biotechnology, 29(6), 361–367 (2002)

    Article  Google Scholar 

  43. AGGARWAL, S. and HOZALSKI, R. M. Determination of biofilm mechanical properties from tensile tests performed using a micro-cantilever method. Biofouling, 26(4), 479–486 (2010)

    Article  Google Scholar 

  44. KORSTGENS, V., FLEMMING, H. C., WINGENDER, J., and BORCHARD, W. Uniaxial compression measurement device for investigation of the mechanical stability of biofilms. Journal of Microbiological Methods, 46(1), 9–17 (2001)

    Article  Google Scholar 

  45. KORSTGENS, V., FLEMMING, H. C., WINGENDER, J., and BORCHARD, W. Influence of calcium ions on the mechanical properties of a model biofilm of mucoid Pseudomonas aeruginosa. Water Science and Technology, 43(6), 49–57 (2001)

    Article  Google Scholar 

  46. ZIENKIEWICZ, O. C. Visco-Plasticity, Plasticity, Creep and Visco-plastic Flow, Lecture Notes in Mathematics, Springer, Berlin (1975)

    Book  MATH  Google Scholar 

  47. YOUNG, F. R. Cavitation, McGraw-Hill, New York (1989)

    Google Scholar 

  48. DOINIKOV, A. A. Translational motion of two interacting bubbles in a strong acoustic field. Physical Review E-Statistical Nonlinear and Soft Matter Physics, 64(2), 026301 (2001)

    Article  Google Scholar 

  49. FONG, S. W., KLASEBOER, E., TURANGAN, C. K., KHOO, B. C., and HUNG, K. C. Numerical analysis of a gas bubble near bio-materials in an ultrasound field. Ultrasound in Medicine and Biology, 32(6), 925–942 (2006)

    Article  Google Scholar 

  50. GUO, X., CAI, C., XU, G., YANG, Y., TU, J., HUANG, P., and ZHANG, D. Interaction between cavitation microbubble and cell: a simulation of sonoporation using boundary element method (BEM). Ultrasonics Sonochemistry, 39, 863–871 (2017)

    Article  Google Scholar 

  51. GUO, C. The Relationship Between the Collapsing Cavitation Bubble and Its Microjet Near a Rigid Wall Under an Ultrasound Field, IntechOpen, London (2018)

    Book  Google Scholar 

  52. JOHNSEN, E. and COLONIUS, T. Numerical simulations of non-spherical bubble collapse. Journal of Fluid Mechanics, 629, 231–262 (2009)

    Article  MathSciNet  MATH  Google Scholar 

  53. MIAO, H. and GRACEWSKI, S. M. Coupled FEM and BEM code for simulating acoustically excited bubbles near deformable structures. Computational Mechanics, 42, 95–106 (2008)

    Article  MATH  Google Scholar 

  54. VYAS, N., MANMI, K., WANG, Q., JADHA, A. J., BARIGOU, M., SAMMONS, R. L., KUEHNE, S. A., and WALMSLEY, A. D. Which parameters affect biofilm removal with acoustic cavitation? a review. Ultrasound in Medicine and Biology, 45(5), 1044–1055 (2019)

    Article  Google Scholar 

  55. BLAKE, J. R., KEEN, G. S., TONG, R. P., and WILSON, M. Acoustic cavitation: the fluid dynamics of non-spherical bubbles. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 357, 251–267 (1999)

    Article  MathSciNet  MATH  Google Scholar 

  56. LAUTERBORN, W. and BOLLE, H. Experimental investigations of cavitation-bubble collapse in the neighbourhood of a solid boundary. Journal of Fluid Mechanics, 72, 391–399 (1975)

    Article  Google Scholar 

  57. RAJARATNAM, N. and MAZUREK, K. A. Impingement of circular turbulent jets on rough boundaries. Journal of Hydraulic Research, 43(6), 689–695 (2005)

    Article  Google Scholar 

  58. BOWER, A. F. Applied Mechanics of Solids, CRC Press, Boca Raton (2009)

    Book  Google Scholar 

  59. BORESI, A. P. and SCHMIDT, R. J. Advanced Mechanics of Materials, Wiley, New York (2003)

    Google Scholar 

  60. DONLAN, R. M. and COSTERTON, W. J. Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews, 15(2), 167–193 (2002)

    Article  Google Scholar 

  61. FROST, H. J. and ASHBY, M. F. Deformation-mechanism Maps: the Plasticity and Creep of Metals and Ceramics, Pergamon Press, New York (1982)

    Google Scholar 

  62. GLOAG, E. S., GERMAN, G. K., STOODLEY, P., and WOZNIAK, D. J. Viscoelastic properties of Pseudomonas aeruginosa variant biofilms. Scientific Reports, 8, 9691 (2018)

    Article  Google Scholar 

  63. PICIOREANU, C., BLAUERT, F., HORN, H., and WAGNER, M. Determination of mechanical properties of biofilms by modelling the deformation measured using optical coherence tomography. Water Research, 145, 588–598 (2018)

    Article  Google Scholar 

  64. AGGARWAL, S., STEWART, P. S., and HOZALSKI, R. M. Biofilm cohesive strength as a basis for biofilm recalcitrance: are bacterial biofilms overdesigned? Microbiology Insights, 8(s2), 29–32 (2015)

    Google Scholar 

  65. EMERENINI, B., HENSE, B. A., KUTTLER, C., and EBERL, H. J. A mathematical model of quorum sensing induced biofilm detachment. PLoS One, 10(7), e0132385 (2015)

    Article  Google Scholar 

  66. FREDERICK, M. R., KUTTLER, C., HENSE, B. A., and EBERL, H. J. A mathematical model of quorum sensing regulated EPS production in biofilms. Theoretical Biology and Medical Modelling, 8, 8 (2011)

    Article  Google Scholar 

  67. EBERL, H. J., PARKER, D. F., and VAN-LOOSDRECHT, C. M. A new deterministic spatiotemporal continuum model for biofilm development. Journal of Theoretical Medicine, 3, 161–175 (2001)

    Article  MATH  Google Scholar 

  68. EBERL, H. J. and DEMARET, L. A finite difference scheme for a degenerated diffusion equation arising in microbial ecology. Electronic Journal of Differential Equations, 15, 77–95 (2007)

    MathSciNet  MATH  Google Scholar 

  69. EFENDIEV, M. A., ZELIK, S. V., and EBERL, H. J. Existence and longtime behavior of a biofilm model. Communications on Pure and Applied Analysis, 8(2), 509–531 (2009)

    Article  MathSciNet  MATH  Google Scholar 

  70. EBERL, H. J. and COLLINSON, S. A modelling and simulation study of siderophore mediated antagonsim in dual-species biofilms. Theoretical Biology and Medical Modelling, 6, 30 (2009)

    Article  Google Scholar 

  71. GHASEMI, M. and EBERL, H. J. Time adaptive numerical solution of a highly degenerate diffusion-reaction biofilm model based on regularisation. Journal of Scientific Computing, 74, 1060–1090 (2018)

    Article  MathSciNet  MATH  Google Scholar 

  72. ENGLMANN, M., FEKETE, A., KUTTLER, C., FROMMBERGER, M., LI, X., GEBEFÜGI, I., FEKETE, J., and SCHMITT-KOPPLIN, P. The hydrolysis of unsubstituted N-acylhomoserine lactones to their homoserine metabolites: analytical approaches using ultra performance liquid chromatography. Journal of Chromatography A, 1160(1–2), 184–193 (2007)

    Article  Google Scholar 

  73. DONG, Y., LI, J., LI, P., and YU, J. Ultrasound microbubbles enhance the activity of vancomycin against staphylococcus epidermidis biofilms in vivo. Journal of Ultrasound in Medicine, 37(6), 1379–1387 (2018)

    Article  Google Scholar 

  74. REUTER, F., LAUTERBORN, S., METTIN, R., and LAUTERBORN, W. Membrane cleaning with ultrasonically driven bubbles. Ultrasonics Sonochemistry, 37, 542–560 (2017)

    Article  Google Scholar 

  75. AGGARWAL, S., POPPELE, E. H., and HOZALSKI, R. M. Development and testing of a novel microcantilever technique for measuring the cohesive strength of intact biofilms. Biotechnology and Bioengineering, 105(5), 924–934 (2009)

    Google Scholar 

  76. MATHIAS, J. D. and STOODLEY, P. Applying the digital image correlation method to estimate the mechanical properties of bacterial biofilms subjected to a wall shear stress. Biofouling, 25(8), 695–703 (2009)

    Article  Google Scholar 

  77. ROCHEX, A., GODON, J. J., BERNET, N., and ESCUDIE, R. Role of shear stress on composition, diversity and dynamics of biofilm bacterial communities. Water Research, 42(20), 4915–4922 (2008)

    Article  Google Scholar 

  78. VAN-WIJNGAARDEN, L. Mechanics of collapsing cavitation bubbles. Ultrasonics Sonochemistry, 29, 524–527 (2016)

    Article  Google Scholar 

  79. WU, T. Y., GUO, N., TEH, C. Y., and HAY, J. X. W. Advances in Ultrasound Technology for Environmental Remediation, Springer, Dordrecht (2013)

    Book  Google Scholar 

  80. CHRISTOPHER, M. R., JOHN, C. C., BENJAMIN, L. B., JARED, L. N., RICHARD, A. R., and WILLIAM, G. P. Low-frequency ultrasound increases outer membrane permeability of Pseudomonas aeruginosa. The Journal of General and Applied Microbiology, 52, 295–301 (2006)

    Article  Google Scholar 

  81. JOHN, C. C., JARED, L. N., BENJAMIN, L. B., CHRISTOPHER, M. R., RICHARD, A. R., and WILLIAM, G. P. Ultrasonic-enhanced gentamicin transport through colony biofilms of Pseudomonas aeruginosa and Escherichia coli. Journal of Infection and Chemotherapy, 10, 193–199 (2004)

    Article  Google Scholar 

  82. DONG, Y. H. and ZHANG, L. H. Quorum sensing and quorum-quenching enzymes. The Journal of Microbiolog, 43(1), 101–109 (2005)

    Google Scholar 

  83. KALIA, V. C. Quorum sensing inhibitors: an overview. Biotechnology Advances, 31(2), 224–245 (2013)

    Article  Google Scholar 

Download references

Acknowledgements

We thank the University of Waterloo for providing financial support.

Author information

Authors and Affiliations

  1. Department of Applied Mathematics, University Waterloo, Waterloo, N2L 3G1, Canada

    M. Ghasemi & S. Sivaloganathan

Authors
  1. M. Ghasemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Sivaloganathan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Ghasemi.

Additional information

Project supported by the Natural Science and Engineering Research Council of Canada (NSERC) with a Discovery Grant (No. PGPIN-04772-2014)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghasemi, M., Sivaloganathan, S. Effect of inertial acoustic cavitation on antibiotic efficacy in biofilms. Appl. Math. Mech.-Engl. Ed. 42, 1397–1422 (2021). https://doi.org/10.1007/s10483-021-2776-7

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10483-021-2776-7

Key words

Chinese Library Classification

2010 Mathematics Subject Classification

Search

Navigation