Advertisement

Ultrasound Cavitation/Microbubble Detection and Medical Applications

  • Zahra Izadifar
  • Paul Babyn
  • Dean Chapman
Review Article

Abstract

Over the past decades, different techniques have been investigated for detecting microbubbles. The purpose of this work is to review the state-of-the-art of medical microbubble detection along with therapeutic, monitoring, and diagnostic applications. The presence of microbubbles in the human body can be induced either through cavitation or exogenous introduction of bubbles. One of the effects of ultrasound is cavitation, or microbubble formation and collapse. Cavitation produces high pressures and temperatures, and microbubble expansion and then collapse close to cells can lead to cellular damage or hemorrhage in biological tissues. Cavitation is, in most cases, an undesired event in clinical diagnostic imaging. Considering that cavitation microbubble formation is largely unpredictable, ultrasound imaging may present a rare or yet unknown risk, particularly to fetuses and embryos. Although most therapeutic ultrasound modalities work based on physical and thermal effects of cavitation, the safety of treatment strongly depends on accurate knowledge of the location of the cavitation inception point. Cavitation detection is an important factor with respect to improving the safety of ultrasound imaging and therapy. It is essential to recognize the existence and location of cavitation inception points. In addition, the use of encapsulated microbubbles as contrast agents for diagnostic imaging, as vehicles for local drug or gene delivery, and as tools for microbubble and ultrasound therapy in thrombolysis has increased the demand for an accurate deep tissue microbubble detection technique. There have been many attempts to detect cavitation bubbles, but each contains its own limitations. There is no doubt that continuous discoveries and developments in microbubble detection modalities will lead to safer and more efficient therapeutic and diagnostic equipment.

Keywords

Ultrasound Detection technique Cavitation bubble Microbubble contrast agent 

Abbreviations

ABI

Analyser based imaging

ACD

Active cavitation detection

BMIT

Biomedical imaging and therapy

CLS

Canadian light source

DPCD

Dual passive cavitation detection

ESR

Electron spin resonance

ESWL

Extracorporeal shock wave lithotripsy

HIFU

High-intensity focused ultrasound

MI

Medical index

MRI

Magnetic resonance imaging

PCD

Passive cavitation detection

PCI

Phase contrast imaging

Notes

Acknowledgements

The authors acknowledge the University of Saskatchewan Dean’s scholarship program (ZI), the Natural Science and Engineering Research Council of Canada (NSERC) Discovery Grant program, and the Canada Research Chairs program (DC).

Author Contributions

ZI wrote and organized the manuscript, PB and DC read and revised the manuscript.

Funding

This work was supported in part by a NSERC Discovery Grant, the Canada Research Chairs Program, and the University of Saskatchewan.

Compliance with Ethical Standards

Conflict of interest

The authors declare that there is no conflict of interest regarding the publication of this paper.

References

  1. 1.
    Cleveland, R. O., & McAteer, J. A. (2012). Extracorporeal shock wave lithotripsy: the physics of shock wave lithotripsy. In B. C. Decker (Ed.), Smith’s Textbook on Endourology. PMPH: Ontario.Google Scholar
  2. 2.
    Chatel, G., & Colmenares, J. C. (2017). Sonochemistry: from basic principles to innovative applications. Topics in Current Chemistry..  https://doi.org/10.1007/s41061-016-0096-1.Google Scholar
  3. 3.
    Holland, C. K., Deng, C. X., Apfel, R. E., Alderman, J. L., Fernandez, L. A., & Taylor, K. J. (1996). Direct evidence of cavitation in vivo from diagnostic ultrasound. Ultrasound in Medicine and Biology, 22(7), 917–925.CrossRefGoogle Scholar
  4. 4.
    Miller, D. L., Smith, N. B., Bailey, M. R., Czarnota, G. J., Hynynen, K., & Makin, I. R. (2012). Overview of therapeutic ultrasound applications and safety considerations. Journal of Ultrasound in Medicine, 31(4), 623–634.CrossRefGoogle Scholar
  5. 5.
    Atchley, A. A., & Prosperetti, A. (1989). The crevice model of bubble nucleation. The Journal of the Acoustical Society of America, 86(3), 1065–1084.  https://doi.org/10.1121/1.398098.CrossRefGoogle Scholar
  6. 6.
    Fuchs, J. (2011) Ultrasonics—Number and Size of Cavitation Bubbles. http://www.ctgclean.com/tech-blog/2011/12/ultrsonics-number-and-size-of-cavitation-bubbles/. Accessed 28 Sept 2015.
  7. 7.
    Leong, T., Ashokkumar, M., & Kentish, S. (2011). The fundamentals of power ultrasound—a review. Acoustics Australia, 39(2), 54–63.Google Scholar
  8. 8.
    Church, C. C., & Carstensen, E. L. (2001). “Stable” inertial cavitation. Ultrasound in Medicine and Biology, 27(10), 1435–1437.CrossRefGoogle Scholar
  9. 9.
    Luque-Garcı́a, J. L., & de Castro, M. D. L. (2003). Ultrasound: a powerful tool for leaching. TrAC Trends in Analytical Chemistry, 22(1), 41–47.  https://doi.org/10.1016/S0165-9936(03)00102-X.CrossRefGoogle Scholar
  10. 10.
    Suslick, K. (1994). The yearbook of science and the future (p. 138). Chicago: Encyclopedia Britannica.Google Scholar
  11. 11.
    Noltingk, B. E., & Neppiras, E. A. (1950). Cavitation produced by ultrasonics. Proceedings of the Physical Society Section B, 63(9), 674.CrossRefGoogle Scholar
  12. 12.
    Plesset, M. (1949). The dynamics of cavitation bubbles. Journal of Applied Mechanics, 16, 277–282.Google Scholar
  13. 13.
    Apfel, R. E., & Holland, C. K. (1991). Gauging the likelihood of cavitation from short-pulse, low-duty cycle diagnostic ultrasound. Ultrasound in Medicine and Biology, 17(2), 179–185.CrossRefGoogle Scholar
  14. 14.
    Holt, R. G., & Roy, R. A. (2001). Measurements of bubble-enhanced heating from focused, MHz-frequency ultrasound in a tissue-mimicking material. Ultrasound in Medicine and Biology, 27(10), 1399–1412.CrossRefGoogle Scholar
  15. 15.
    Nyborg, W. L. (1998). Acoustic streaming nonlinear acoustics. San Diego: Academic Press.Google Scholar
  16. 16.
    Dijkmans, P. A., Juffermans, L. J., Musters, R. J., van Wamel, A., ten Cate, F. J., van Gilst, W., et al. (2004). Microbubbles and ultrasound: from diagnosis to therapy. Eur J Echocardiogr., 5(4), 245–256.  https://doi.org/10.1016/j.euje.2004.02.001.CrossRefGoogle Scholar
  17. 17.
    Skyba, D. M., Price, R. J., Linka, A. Z., Skalak, T. C., & Kaul, S. (1998). Direct in vivo visualization of intravascular destruction of microbubbles by ultrasound and its local effects on tissue. Circulation, 98(4), 290–293.CrossRefGoogle Scholar
  18. 18.
    Nejad, S. M., Hosseini, H., Akiyama, H., & Tachibana, K. (2016). Reparable cell sonoporation in suspension: theranostic potential of microbubble. Theranostics, 6(4), 446.CrossRefGoogle Scholar
  19. 19.
    Fan, Z., Chen, D., & Deng, C. (2013). Improving ultrasound gene transfection efficiency by controlling ultrasound excitation of microbubbles. Journal of Controlled Release, 170(3), 401–413.CrossRefGoogle Scholar
  20. 20.
    Helfield, B., Chen, X., Watkins, S. C., & Villanueva, F. S. (2016). Biophysical insight into mechanisms of sonoporation. Proceedings of the National Academy of Sciences, 113(36), 9983–9988.CrossRefGoogle Scholar
  21. 21.
    Matlaga, B. R., McAteer, J. A., Connors, B. A., Handa, R. K., Evan, A. P., Williams, J. C., et al. (2008). Potential for cavitation-mediated tissue damage in shockwave lithotripsy. Journal of Endourology, 22(1), 121–126.CrossRefGoogle Scholar
  22. 22.
    Lawrie, A., Brisken, A. F., Francis, S. E., Tayler, D. I., Chamberlain, J., Crossman, D. C., et al. (1999). Ultrasound enhances reporter gene expression after transfection of vascular cells in vitro. Circulation, 99(20), 2617–2620.CrossRefGoogle Scholar
  23. 23.
    Stride, E., & Saffari, N. (2003). On the destruction of microbubble ultrasound contrast agents. Ultrasound in Medicine and Biology, 29(4), 563–573.  https://doi.org/10.1016/s0301-5629(02)00787-1.CrossRefGoogle Scholar
  24. 24.
    Hernot, S., & Klibanov, A. L. (2008). Microbubbles in ultrasound-triggered drug and gene delivery. Advanced Drug Delivery Reviews, 60(10), 1153–1166.  https://doi.org/10.1016/j.addr.2008.03.005.CrossRefGoogle Scholar
  25. 25.
    Basta, G., Venneri, L., Lazzerini, G., Pasanisi, E., Pianelli, M., Vesentini, N., et al. (2003). In vitro modulation of intracellular oxidative stress of endothelial cells by diagnostic cardiac ultrasound. Cardiovascular Research, 58(1), 156–161.CrossRefGoogle Scholar
  26. 26.
    Ferrara, K., Pollard, R., & Borden, M. (2007). Ultrasound microbubble contrast agents: fundamentals and application to gene and drug delivery. Annual Review of Biomedical Engineering, 9, 415–447.  https://doi.org/10.1146/annurev.bioeng.8.061505.095852.CrossRefGoogle Scholar
  27. 27.
    Nanda, N., Schlief, R., & Goldberg, B. B. (1997). Advances in echo imagingusing contrast enhancement (2nd ed.). Dordrecht: Kluwer Academic.CrossRefGoogle Scholar
  28. 28.
    Mayer, S., & Grayburn, P. A. (2001). Myocardial contrast agents: recent advances and future directions. Progress in Cardiovascular Diseases, 44(1), 33–44.  https://doi.org/10.1053/pcad.2001.26438.CrossRefGoogle Scholar
  29. 29.
    Bouakaz, A., de Jong, N., Cachard, C., & Jouini, K. (1998). On the effect of lung filtering and cardiac pressure on the standard properties of ultrasound contrast agent. Ultrasonics, 36(1–5), 703–708.CrossRefGoogle Scholar
  30. 30.
    Unger, E. C., Hersh, E., Vannan, M., Matsunaga, T. O., & McCreery, M. (2001). Local drug and gene delivery through microbubbles. Progress in Cardiovascular Diseases, 44(1), 45–54.  https://doi.org/10.1053/pcad.2001.26443.CrossRefGoogle Scholar
  31. 31.
    Mulvagh, S. L., DeMaria, A. N., Feinstein, S. B., Burns, P. N., Kaul, S., Miller, J. G., et al. (2000). Contrast echocardiography: Current and future applications. Journal of the American Society of Echocardiography, 13(4), 331–342.  https://doi.org/10.1067/mje.2000.105462.CrossRefGoogle Scholar
  32. 32.
    Liang, H., Tang, J., & Halliwell, M. (2010). Sonoporation, drug delivery, and gene therapy. Proceedings of the Institution of Mechanical Engineers, Part H, Journal of Engineering in Medicine, 224(2), 343–361.CrossRefGoogle Scholar
  33. 33.
    Collis, J., Manasseh, R., Liovic, P., Tho, P., Ooi, A., Petkovic-Duran, K., et al. (2010). Cavitation microstreaming and stress fields created by microbubbles. Ultrasonics, 50(2), 273–279.CrossRefGoogle Scholar
  34. 34.
    Wu, J., Ross, J. P., & Chiu, J.-F. (2002). Reparable sonoporation generated by microstreaming. The Journal of the Acoustical Society of America., 111(3), 1460–1464.CrossRefGoogle Scholar
  35. 35.
    Liu, H.-L., Fan, C.-H., Ting, C.-Y., & Yeh, C.-K. (2014). Combining microbubbles and ultrasound for drug delivery to brain tumors: current progress and overview. Theranostics., 4(4), 432.CrossRefGoogle Scholar
  36. 36.
    Chu, P. C., Liu, H. L., Lai, H. Y., Lin, C. Y., Tsai, H. C., & Pei, Y. C. (2015). Neuromodulation accompanying focused ultrasound-induced blood-brain barrier opening. Scientific Reports, 5, 15477.  https://doi.org/10.1038/srep15477.CrossRefGoogle Scholar
  37. 37.
    Yoo, S.-S., Bystritsky, A., Lee, J.-H., Zhang, Y., Fischer, K., Min, B.-K., et al. (2011). Focused ultrasound modulates region-specific brain activity. Neuroimage., 56(3), 1267–1275.CrossRefGoogle Scholar
  38. 38.
    Bystritsky, A., Korb, A. S., Douglas, P. K., Cohen, M. S., Melega, W. P., Mulgaonkar, A. P., et al. (2011). A review of low-intensity focused ultrasound pulsation. Brain Stimulation, 4(3), 125–136.  https://doi.org/10.1016/j.brs.2011.03.007.CrossRefGoogle Scholar
  39. 39.
    Rezayat, E., & Toostani, I. G. (2016). A review on brain stimulation using low intensity focused ultrasound. Basic and Clinical Neuroscience., 7(3), 187.Google Scholar
  40. 40.
    Hynynen, K., McDannold, N., Vykhodtseva, N., & Jolesz, F. A. (2001). Noninvasive MR imaging guided focal opening of the blood-brain barrier in rabbits 1. Radiology, 220(3), 640–646.CrossRefGoogle Scholar
  41. 41.
    Chu, P. C., Chai, W. Y., Tsai, C. H., Kang, S. T., Yeh, C. K., & Liu, H. L. (2016). Focused ultrasound-induced blood-brain barrier opening: association with mechanical index and cavitation index analyzed by dynamic contrast-enhanced magnetic-resonance imaging. Scientific Reports, 6, 33264.  https://doi.org/10.1038/srep33264.CrossRefGoogle Scholar
  42. 42.
    Porter, T. R., Hiser, W. L., Kricsfeld, D., Deligonul, U., Xie, F., Iversen, P., et al. (2001). Inhibition of carotid artery neointimal formation with intravenous microbubbles. Ultrasound in Medicine and Biology, 27(2), 259–265.CrossRefGoogle Scholar
  43. 43.
    Price, R. J., & Kaul, S. (2002). Contrast ultrasound targeted drug and gene delivery: an update on a new therapeutic modality. J Cardiovascular Pharmacology Therapy, 7(3), 171–180.CrossRefGoogle Scholar
  44. 44.
    Ng, K. Y., & Liu, Y. (2002). Therapeutic ultrasound: its application in drug delivery. Medicinal Research Reviews, 22(2), 204–223.  https://doi.org/10.1002/med.10004.CrossRefGoogle Scholar
  45. 45.
    Lindner, J. R. (2002). Evolving applications for contrast ultrasound. American Journal of Cardiology, 90(10A), 72J–80J.CrossRefGoogle Scholar
  46. 46.
    Unger, E. C., Matsunaga, T. O., McCreery, T., Schumann, P., Sweitzer, R., & Quigley, R. (2002). Therapeutic applications of microbubbles. European Journal of Radiology, 42(2), 160–168.  https://doi.org/10.1016/s0720-048x(01)00455-7.CrossRefGoogle Scholar
  47. 47.
    Tachibana, K., & Tachibana, S. (2001). The use of ultrasound for drug delivery. Echocardiography, 18(4), 323–328.  https://doi.org/10.1046/j.1540-8175.2001.00323.x.CrossRefGoogle Scholar
  48. 48.
    Lindner, J. R., & Kaul, S. (2001). Delivery of drugs with ultrasound. Echocardiography, 18(4), 329–337.  https://doi.org/10.1046/j.1540-8175.2001.00329.x.CrossRefGoogle Scholar
  49. 49.
    McDannold, N., Arvanitis, C. D., Vykhodtseva, N., & Livingstone, M. S. (2012). Temporary disruption of the blood–brain barrier by use of ultrasound and microbubbles: safety and efficacy evaluation in rhesus macaques. Cancer Research, 72(14), 3652–3663.CrossRefGoogle Scholar
  50. 50.
    Hynynen, K., McDannold, N., Vykhodtseva, N., Raymond, S., Weissleder, R., Jolesz, F. A., et al. (2006). Focal disruption of the blood–brain barrier due to 260-kHz ultrasound bursts: a method for molecular imaging and targeted drug delivery. Journal of Neurosurgery, 105(3), 445–454.CrossRefGoogle Scholar
  51. 51.
    Tartis, M. S., McCallan, J., Lum, A. F., LaBell, R., Stieger, S. M., Matsunaga, T. O., et al. (2006). Therapeutic effects of paclitaxel-containing ultrasound contrast agents. Ultrasound in Medicine and Biology, 32(11), 1771–1780.  https://doi.org/10.1016/j.ultrasmedbio.2006.03.017.CrossRefGoogle Scholar
  52. 52.
    Chen, S., J-h, Ding, Bekeredjian, R., B-z, Yang, Shohet, R. V., Johnston, S. A., et al. (2006). Efficient gene delivery to pancreatic islets with ultrasonic microbubble destruction technology. Proceedings of the National Academy of Sciences, 103(22), 8469–8474.CrossRefGoogle Scholar
  53. 53.
    Hauff, P., Seemann, S., Reszka, R., Schultze-Mosgau, M., Reinhardt, M., Buzasi, T., et al. (2005). Evaluation of gas-filled microparticles and sonoporation as gene delivery system: feasibility study in rodent tumor models 1. Radiology, 236(2), 572–578.CrossRefGoogle Scholar
  54. 54.
    Price, R. J., Skyba, D. M., Kaul, S., & Skalak, T. C. (1998). Delivery of colloidal particles and red blood cells to tissue through microvessel ruptures created by targeted microbubble destruction with ultrasound. Circulation, 98(13), 1264–1267.CrossRefGoogle Scholar
  55. 55.
    Miller, D. L., & Quddus, J. (2000). Diagnostic ultrasound activation of contrast agent gas bodies induces capillary rupture in mice. Proceedings of the National Academy of Sciences, 97(18), 10179–10184.CrossRefGoogle Scholar
  56. 56.
    Dimcevski, G., Kotopoulis, S., Bjånes, T., Hoem, D., Schjøtt, J., Gjertsen, B. T., et al. (2016). A human clinical trial using ultrasound and microbubbles to enhance gemcitabine treatment of inoperable pancreatic cancer. Journal of Controlled Release, 243, 172–181.CrossRefGoogle Scholar
  57. 57.
    Kotopoulis, S., Dimcevski, G., Gilja, O. H., Hoem, D., & Postema, M. (2013). Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: a clinical case study. Medical Physics, 40(7), 072902.CrossRefGoogle Scholar
  58. 58.
    Wu, J. R. (1998). Temperature rise generated by ultrasound in the presence of contrast agent. Ultrasound in Medicine and Biology, 24(2), 267–274.  https://doi.org/10.1016/s0301-5629(97)00246-9.MathSciNetCrossRefGoogle Scholar
  59. 59.
    Miller, D. L., & Gies, R. A. (1998). Enhancement of ultrasonically-induced hemolysis by perfluorocarbon-based compared to air-based echo-contrast agents. Ultrasound in Medicine and Biology, 24(2), 285–292.  https://doi.org/10.1016/s0301-5629(97)00267-6.CrossRefGoogle Scholar
  60. 60.
    Poliachik, S. L., Chandler, W. L., Mourad, P. D., Bailey, M. R., Bloch, S., Cleveland, R. O., et al. (1999). Effect of high-intensity focused ultrasound on whole blood with and without microbubble contrast agent. Ultrasound in Medicine and Biology, 25(6), 991–998.  https://doi.org/10.1016/s0301-5629(99)00043-5.CrossRefGoogle Scholar
  61. 61.
    Bekeredjian, R., Chen, S., Frenkel, P. A., Grayburn, P. A., & Shohet, R. V. (2003). Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation, 108(8), 1022–1026.  https://doi.org/10.1161/01.cir.0000084535.35435.ae.CrossRefGoogle Scholar
  62. 62.
    Frenkel, P. A., Chen, S., Thai, T., Shohet, R. V., & Grayburn, P. A. (2002). DNA-loaded albumin microbubbles enhance ultrasound-mediated transfection in vitro. Ultrasound in Medicine and Biology, 28(6), 817–822.CrossRefGoogle Scholar
  63. 63.
    Shohet, R. V., Chen, S., Zhou, Y. T., Wang, Z., Meidell, R. S., Unger, R. H., et al. (2000). Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium. Circulation, 101(22), 2554–2556.CrossRefGoogle Scholar
  64. 64.
    Smeenge, M., Tranquart, F., Mannaerts, C. K., de Reijke, T. M., van de Vijver, M. J., Laguna, M. P., et al. (2017). first-in-human ultrasound molecular imaging with a VEGFR2-specific ultrasound molecular contrast agent (BR55) in prostate cancer: a safety and feasibility pilot study. Investigative Radiology, 52, 419.CrossRefGoogle Scholar
  65. 65.
    Willmann, J. K., Bonomo, L., Carla Testa, A., Rinaldi, P., Rindi, G., Valluru, K. S., et al. (2017). Ultrasound molecular imaging with BR55 in patients with breast and ovarian lesions: first-in-human results. Journal of Clinical Oncology, 35, 2133.CrossRefGoogle Scholar
  66. 66.
    Villanueva, F. S., Jankowski, R. J., Klibanov, S., Pina, M. L., Alber, S. M., Watkins, S. C., et al. (1998). Microbubbles targeted to intercellular adhesion molecule-1 bind to activated coronary artery endothelial cells. Circulation, 98(1), 1–5.CrossRefGoogle Scholar
  67. 67.
    Weller, G. E., Lu, E., Csikari, M. M., Klibanov, A. L., Fischer, D., Wagner, W. R., et al. (2003). Ultrasound imaging of acute cardiac transplant rejection with microbubbles targeted to intercellular adhesion molecule-1. Circulation, 108(2), 218–224.  https://doi.org/10.1161/01.cir.0000080287.74762.60.CrossRefGoogle Scholar
  68. 68.
    Ellegala, D. B., Leong-Poi, H., Carpenter, J. E., Klibanov, A. L., Kaul, S., Shaffrey, M. E., et al. (2003). Imaging tumor angiogenesis with contrast ultrasound and microbubbles targeted to alpha(v)beta3. Circulation, 108(3), 336–341.  https://doi.org/10.1161/01.cir.0000080326.15367.0c.CrossRefGoogle Scholar
  69. 69.
    Lindner, J. R., Coggins, M. P., Kaul, S., Klibanov, A. L., Brandenburger, G. H., & Ley, K. (2000). Microbubble persistence in the microcirculation during ischemia/reperfusion and inflammation is caused by integrin- and complement-mediated adherence to activated leukocytes. Circulation, 101(6), 668–675.CrossRefGoogle Scholar
  70. 70.
    Lindner, J. R., Dayton, P. A., Coggins, M. P., Ley, K., Song, J., Ferrara, K., et al. (2000). Noninvasive imaging of inflammation by ultrasound detection of phagocytosed microbubbles. Circulation, 102(5), 531–538.CrossRefGoogle Scholar
  71. 71.
    Christiansen, J. P., Leong-Poi, H., Klibanov, A. L., Kaul, S., & Lindner, J. R. (2002). Noninvasive imaging of myocardial reperfusion injury using leukocyte-targeted contrast echocardiography. Circulation, 105(15), 1764–1767.CrossRefGoogle Scholar
  72. 72.
    Schumann, P. A., Christiansen, J. P., Quigley, R. M., McCreery, T. P., Sweitzer, R. H., Unger, E. C., et al. (2002). Targeted-microbubble binding selectively to GPIIb IIIa receptors of platelet thrombi. Investigative Radiology, 37(11), 587–593.  https://doi.org/10.1097/01.rli.0000031077.17751.b2.CrossRefGoogle Scholar
  73. 73.
    Akiyama, M., Ishibashi, T., Yamada, T., & Furuhata, H. (1998). Low-frequency ultrasound penetrates the cranium and enhances thrombolysis in vitro. Neurosurgery., 43(4), 828–832.  https://doi.org/10.1097/00006123-199810000-00062.CrossRefGoogle Scholar
  74. 74.
    Harpaz, D., Chen, X. C., Francis, C. W., Marder, V. J., & Meltzer, R. S. (1993). Ultrasound enhancement of thrombolysis and reperfusion in vitro. Journal of the American College of Cardiology, 21(6), 1507–1511.CrossRefGoogle Scholar
  75. 75.
    Kornowski, R., Meltzer, R. S., Chernine, A., Vered, Z., & Battler, A. (1994). Does external ultrasound accelerate thrombolysis? Results from a rabbit model. Circulation., 89(1), 339–344.CrossRefGoogle Scholar
  76. 76.
    Larsson, J., Carlson, J., & Olsson, S. B. (1998). Ultrasound enhanced thrombolysis in experimental retinal vein occlusion in the rabbit. British Journal of Ophthalmology, 82(12), 1438–1440.  https://doi.org/10.1136/bjo.82.12.1438.CrossRefGoogle Scholar
  77. 77.
    Lauer, C. G., Burge, R., Tang, D. B., Bass, B. G., Gomez, E. R., & Alving, B. M. (1992). Effect of ultrasound on tissue-type plasminogen activator-induced thrombolysis. Circulation, 86(4), 1257–1264.CrossRefGoogle Scholar
  78. 78.
    Luo, H., Nishioka, T., Fishbein, M. C., Cercek, B., Forrester, J. S., Kim, C. J., et al. (1996). Transcutaneous ultrasound augments lysis of arterial thrombi in vivo. Circulation, 94(4), 775–778.CrossRefGoogle Scholar
  79. 79.
    Riggs, P. N., Francis, C. W., Bartos, S. R., & Penney, D. P. (1997). Ultrasound enhancement of rabbit femoral artery thrombolysis. Cardiovascular Surgery, 5(2), 201–207.CrossRefGoogle Scholar
  80. 80.
    Rassin, T., Desmet, W., Piessens, J., & Rosenschein, U. (2000). Ultrasound thrombolysis in stent thrombosis. Catheterization and Cardiovascular Interventions, 51(3), 332–334.CrossRefGoogle Scholar
  81. 81.
    Porter, T. R., & Xie, F. (2001). Ultrasound, microbubbles, and thrombolysis. Progress in Cardiovascular Diseases, 44(2), 101–110.  https://doi.org/10.1053/pcad.2001.26441.CrossRefGoogle Scholar
  82. 82.
    Tachibana, K., & Tachibana, S. (1995). Albumin microbubble echo-contrast material as an enhancer for ultrasound accelerated thrombolysis. Circulation, 92(5), 1148–1150.CrossRefGoogle Scholar
  83. 83.
    Kondo, I., Mizushige, K., Ueda, T., Masugata, H., Ohmori, K., & Matsuo, H. (1999). Histological observations and the process of ultrasound contrast agent enhancement of tissue plasminogen activator thrombolysis with ultrasound exposure. Japanese Circulation Journal, 63(6), 478–484.CrossRefGoogle Scholar
  84. 84.
    Nishioka, T., Luo, H., Fishbein, M. C., Cercek, B., Forrester, J. S., Kim, C. J., et al. (1997). Dissolution of thrombotic arterial occlusion by high intensity, low frequency ultrasound and dodecafluoropentane emulsion: An in vitro and in vivo study. Journal of the American College of Cardiology, 30(2), 561–568.  https://doi.org/10.1016/s0735-1097(97)00182-4.CrossRefGoogle Scholar
  85. 85.
    Porter, T. R., LeVeen, R. F., Fox, R., Kricsfeld, A., & Xie, F. (1996). Thrombolytic enhancement with perfluorocarbon-exposed sonicated dextrose albumin microbubbles. American Heart Journal, 132(5), 964–968.  https://doi.org/10.1016/s0002-8703(96)90006-x.CrossRefGoogle Scholar
  86. 86.
    Mizushige, K., Kondo, I., Ohmori, K., Hirao, K., & Matsuo, H. (1999). Enhancement of ultrasound-accelerated thrombolysis by echo contrast agents: dependence on microbubble structure. Ultrasound in Medicine and Biology, 25(9), 1431–1437.  https://doi.org/10.1016/s0301-5629(99)00095-2.CrossRefGoogle Scholar
  87. 87.
    Nacu, A., Kvistad, C. E., Naess, H., Øygarden, H., Logallo, N., Assmus, J., et al. (2016). NOR-SASS (Norwegian Sonothrombolysis in Acute Stroke Study). Stroke, 48, 335.CrossRefGoogle Scholar
  88. 88.
    Kobayashi, N., Yasu, T., Yamada, S., Kudo, N., Kuroki, M., Kawakami, M., et al. (2002). Endothelial cell injury in venule and capillary induced by contrast ultrasonography. Ultrasound in Medicine and Biology, 28(7), 949–956.  https://doi.org/10.1016/s0301-5629(02)00532-x.CrossRefGoogle Scholar
  89. 89.
    Cootney, R. W. (2001). Ultrasound imaging: principles and applications in rodent research. ILAR Journal, 42(3), 233–247.CrossRefGoogle Scholar
  90. 90.
    O’Reilly, M. A., Hough, O., & Hynynen, K. (2017). Blood-brain barrier closure time after controlled ultrasound-induced opening is independent of opening volume. Journal of Ultrasound in Medicine, 36(3), 475–483.CrossRefGoogle Scholar
  91. 91.
    Holland, C. K., Deng, C. X., Apfel, R. E., Alderman, J. L., Fernandez, L. A., & Taylor, K. J. (1996). Direct evidence of cavitation in vivo from diagnostic ultrasound. Ultrasound in Medicine and Biology, 22(7), 917–925.CrossRefGoogle Scholar
  92. 92.
    Bailey, M. R., Pishchalnikov, Y. A., Sapozhnikov, O. A., Cleveland, R. O., McAteer, J. A., Miller, N. A., et al. (2005). Cavitation detection during shock-wave lithotripsy. Ultrasound in Medicine and Biology, 31(9), 1245–1256.  https://doi.org/10.1016/j.ultrasmedbio.2005.02.017.CrossRefGoogle Scholar
  93. 93.
    Leighton, T. G. (1994). The acoustic bubble. San Diego: Academic Press.Google Scholar
  94. 94.
    Matula, T. J., Hilmo, P. R., Bailey, M. R., & Crum, L. A. (2002). In vitro sonoluminescence and sonochemistry studies with an electrohydraulic shock-wave lithotripter. Ultrasound in Medicine and Biology, 28(9), 1199–1207.CrossRefGoogle Scholar
  95. 95.
    Coleman, A. J., Whitlock, M., Leighton, T., & Saunders, J. E. (1993). The spatial distribution of cavitation induced acoustic emission, sonoluminescence and cell lysis in the field of a shock wave lithotripter. Physics in Medicine and Biology, 38(11), 1545–1560.CrossRefGoogle Scholar
  96. 96.
    Pye, S. D., & Dineley, J. A. (1999). Characterization of cavitational activity in lithotripsy fields using a robust electromagnetic probe. Ultrasound in Medicine and Biology, 25(3), 451–471.CrossRefGoogle Scholar
  97. 97.
    Atchley, A., Frizzell, L., Apfel, R., Holland, C., Madanshetty, S., & Roy, R. (1988). Thresholds for cavitation produced in water by pulsed ultrasound. Ultrasonics, 26(5), 280–285.CrossRefGoogle Scholar
  98. 98.
    Chen, H. (2011). ultra-high speed optical imaging of ultrasound-activated microbubbles in mesenteric microvessels. Washington, DC: University of Washington.Google Scholar
  99. 99.
    Philipp, A., Delius, M., Scheffczyk, C., Vogel, A., & Lauterborn, W. (1993). Interaction of lithotripter-generated shock waves with air bubbles. The Journal of the Acoustical Society of America., 93(5), 2496–2509.  https://doi.org/10.1121/1.406853.CrossRefGoogle Scholar
  100. 100.
    Zhong, P., Cioanta, I., Cocks, F. H., & Preminger, G. M. (1997). Inertial cavitation and associated acoustic emission produced during electrohydraulic shock wave lithotripsy. Journal of the Acoustical Society of America, 101(5 Pt 1), 2940–2950.CrossRefGoogle Scholar
  101. 101.
    Pishchalnikov, Y. A., Sapozhnikov, O. A., Bailey, M. R., Williams, J. C., Jr., Cleveland, R. O., Colonius, T., et al. (2003). Cavitation bubble cluster activity in the breakage of kidney stones by lithotripter shockwaves. Journal of Endourology, 17(7), 435–446.  https://doi.org/10.1089/089277903769013568.CrossRefGoogle Scholar
  102. 102.
    Tomita, Y., & Shima, A. (1990). High-speed photographic observations of laser-induced cavitation bubbles in water. Acta Acustica United with Acustica., 71(3), 161–171.Google Scholar
  103. 103.
    Ibsen, S., Benchimol, M., & Esener, S. (2013). Fluorescent microscope system to monitor real-time interactions between focused ultrasound, echogenic drug delivery vehicles, and live cell membranes. Ultrasonics, 53(1), 178–184.  https://doi.org/10.1016/j.ultras.2012.05.006.CrossRefGoogle Scholar
  104. 104.
    Ibsen, S., Benchimol, M., Simberg, D., Schutt, C., Steiner, J., & Esener, S. (2011). A novel nested liposome drug delivery vehicle capable of ultrasound triggered release of its payload. Journal of Controlled Release, 155(3), 358–366.  https://doi.org/10.1016/j.jconrel.2011.06.032.CrossRefGoogle Scholar
  105. 105.
    Chomas, J. E., Dayton, P., May, D., & Ferrara, K. (2001). Threshold of fragmentation for ultrasonic contrast agents. Journal of Biomedial Optics, 6(2), 141–150.  https://doi.org/10.1117/1.1352752.CrossRefGoogle Scholar
  106. 106.
    Brahme, A. (2014). Comprehensive biomedical physics. Amsterdam: Elsevier Science.Google Scholar
  107. 107.
    Peng, H. H., Wu, C. H., Kang, S. T., Zhang, J. W., Liu, H. L., Chen, W. S., et al. (2017). Real-time monitoring of inertial cavitation effects of microbubbles by using MRI: in vitro experiments. Magnetic Resonance in Medicine, 77(1), 102–111.CrossRefGoogle Scholar
  108. 108.
    Coakley, W. (1971). Acoustical detection of single cavitation events in a focused field in water at 1 MHz. The Journal of the Acoustical Society of America., 49(3B), 792–801.CrossRefGoogle Scholar
  109. 109.
    Roy, R. A., Madanshetty, S. I., & Apfel, R. E. (1990). An acoustic backscattering technique for the detection of transient cavitation produced by microsecond pulses of ultrasound. The Journal of the Acoustical Society of America., 87(6), 2451–2458.  https://doi.org/10.1121/1.399091.CrossRefGoogle Scholar
  110. 110.
    Madanshetty, S. I., Roy, R. A., & Apfel, R. E. (1991). Acoustic microcavitation: its active and passive acoustic detection. Journal of the Acoustical Society of America, 90(3), 1515–1526.CrossRefGoogle Scholar
  111. 111.
    Cleveland, R. O., Sapozhnikov, O. A., Bailey, M. R., & Crum, L. A. (2000). A dual passive cavitation detector for localized detection of lithotripsy-induced cavitation in vitro. Journal of the Acoustical Society of America, 107(3), 1745–1758.CrossRefGoogle Scholar
  112. 112.
    Hockham, N., Coussios, C. C., & Arora, M. (2010). A real-time controller for sustaining thermally relevant acoustic cavitation during ultrasound therapy. IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, 57(12), 2685–2694.  https://doi.org/10.1109/tuffc.2010.1742.CrossRefGoogle Scholar
  113. 113.
    Salgaonkar, V. A. (2009). Passive imaging and measurements of acoustic cavitation during ultrasound ablation. Cincinnati: University of Cincinnati.Google Scholar
  114. 114.
    Gyöngy, M., & Coussios, C.-C. (2010). Passive cavitation mapping for localization and tracking of bubble dynamics. The Journal of the Acoustical Society of America, 128(4), 175–180.CrossRefGoogle Scholar
  115. 115.
    Haworth, K. J., Mast, T. D., Radhakrishnan, K., Burgess, M. T., Kopechek, J. A., Huang, S. L., et al. (2012). Passive imaging with pulsed ultrasound insonations. Journal of the Acoustical Society of America, 132(1), 544–553.  https://doi.org/10.1121/1.4728230.CrossRefGoogle Scholar
  116. 116.
    Delius, M., & Gambihler, S. (1992). Sonographic imaging of extracorporeal shock wave effects in the liver and gallbladder of dogs. Digestion., 52(1), 55–60.CrossRefGoogle Scholar
  117. 117.
    Coleman, A. J., Choi, M. J., & Saunders, J. E. (1996). Detection of acoustic emission from cavitation in tissue during clinical extracorporeal lithotripsy. Ultrasound in Medicine and Biology, 22(8), 1079–1087.CrossRefGoogle Scholar
  118. 118.
    Coussios, C., Farny, C., Ter Haar, G., & Roy, R. (2007). Role of acoustic cavitation in the delivery and monitoring of cancer treatment by high-intensity focused ultrasound (HIFU). International Journal of Hyperthermia, 23(2), 105–120.CrossRefGoogle Scholar
  119. 119.
    Sapozhnikov, O.A., Bailey, M.R., Crum, L.A., Miller, N.A., Cleveland, R.O., Pishchalnikov, Y.A. et al. (2001) Ultrasound-guided localized detection of cavitation during lithotripsy in pig kidney in vivo. Ultrasonics symposium.Google Scholar
  120. 120.
    Duck, F. A. (1999). Acoustic saturation and output regulation. Ultrasound in Medicine and Biology, 25(6), 1009–1018.CrossRefGoogle Scholar
  121. 121.
    Radiation Tiagon-i (2010) Health effects of exposure to ultrasound and infrasound. In Documents of the health protection agency, radiation, chemical and environmental hazards.Google Scholar
  122. 122.
    Arfelli, F., Rigon, L., & Menk, R. (2010). Microbubbles as X-ray scattering contrast agents using analyzer-based imaging. Physics in Medicine and Biology, 55(6), 1643.CrossRefGoogle Scholar
  123. 123.
    Millard, T., Endrizzi, M., Rigon, L., Arfelli, F., Menk, R., Owen, J., et al. (2013). Quantification of microbubble concentration through X-ray phase contrast imaging. Applied Physics Letters, 103(11), 114105.CrossRefGoogle Scholar
  124. 124.
    Izadifar, Z., Belev, G., Izadifar, M., Izadifar, Z., & Chapman, D. (2014). Visualization of ultrasound induced cavitation bubbles using the synchrotron X-ray analyzer based imaging technique. Physics in Medicine and Biology, 59(23), 7541.CrossRefGoogle Scholar
  125. 125.
    Izadifar, Z., Belev, G., Babyn, P., & Chapman, D. (2015). Application of analyzer based X-ray imaging technique for detection of ultrasound induced cavitation bubbles from a physical therapy unit. Biomedical Engineering Online., 14(1), 91.CrossRefGoogle Scholar
  126. 126.
    Stride, E. P., & Coussios, C. C. (2010). Cavitation and contrast: the use of bubbles in ultrasound imaging and therapy. Proceedings of the Institution of Mechanical Engineers, Part H, 224(2), 171–191.CrossRefGoogle Scholar
  127. 127.
    Health effects of exposure to ultrasound and infrasound. Health Protection Agency 2010. Report No.: RCE-14, Contract No.: 978-0-85951-662-4.Google Scholar
  128. 128.
    Carmichael, A. J., Mossoba, M. M., Riesz, P., & Christman, C. L. (1986). Free radical production in aqueous solutions exposed to simulated ultrasonic diagnostic conditions. IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, 33(2), 148–155.CrossRefGoogle Scholar
  129. 129.
    Crum, L., & Fowlkes, J. (1986). Acoustic cavitation generated by microsecond pulses of ultrasound. Nature, 319, 52–54.CrossRefGoogle Scholar
  130. 130.
    Coleman, A. J., Saunders, J. E., Crum, L. A., & Dyson, M. (1987). Acoustic cavitation generated by an extracorporeal shockwave lithotripter. Ultrasound in Medicine and Biology, 13(2), 69–76.CrossRefGoogle Scholar
  131. 131.
    Bailey, M. R., Blackstock, D. T., Cleveland, R. O., & Crum, L. A. (1998). Comparison of electrohydraulic lithotripters with rigid and pressure-release ellipsoidal reflectors. I. Acoustic fields. The Journal of the Acoustical Society of America, 104(4), 2517–2524.CrossRefGoogle Scholar
  132. 132.
    Lifshitz, D. A., Williams Jr, J. C., Sturtevant, B., Connors, B. A., Evan, A. P., & McAteer, J. A. (1997). Quantitation of shock wave cavitation damage in vitro. Ultrasound in Medicine & Biology, 23(3), 461–471.  https://doi.org/10.1016/S0301-5629(96)00223-2.CrossRefGoogle Scholar
  133. 133.
    Zijlstra, A., Janssens, T., Wostyn, K., Versluis, M., Mertens, P. W., & Lohse, D. (Eds.). (2009). High speed imaging of 1 MHz driven microbubbles in contact with a rigid wall. In Solid state phenomena. Trans Tech Publ.Google Scholar
  134. 134.
    Vignon, F., Shi, W. T., Powers, J. E., Everbach, E. C., Liu, J., Gao, S., et al. (2013). Microbubble cavitation imaging. IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, 60(4), 661–670.CrossRefGoogle Scholar

Copyright information

© Taiwanese Society of Biomedical Engineering 2018

Authors and Affiliations

  1. 1.Division of Biomedical Engineering, College of EngineeringUniversity of SaskatchewanSaskatoonCanada
  2. 2.Department of Medical Imaging, University of Saskatchewan and Saskatoon Health RegionRoyal University HospitalSaskatoonCanada
  3. 3.Anatomy and Cell BiologyUniversity of SaskatchewanSaskatoonCanada

Personalised recommendations