A review of in vitro bioeffects of inertial ultrasonic cavitation from a mechanistic perspective

Ultrasound in Medicine and Biology

Volumn 22, Issue 9, 1996, Pages 1131-1154

  Miller, Morton W ^a   Miller, Douglas L ^b   Brayman, Andrew A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUBBLES (IN FLUIDS); CAVITATION; CELLS;

BIOEFFECTS; ULTRASONIC CAVITATION;

ULTRASONIC EFFECTS;

ANIMAL CELL; CELL VIABILITY; CYTOLYSIS; ECHOGRAPHY; LITHOTRIPSY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SOUND INTENSITY; SOUND PRESSURE; SOUND TRANSMISSION; ULTRAVIOLET RADIATION; X RAY;

ANIMALS; BIOPHYSICS; CELL DEATH; CELL DIVISION; CELL PHYSIOLOGY; CELL SURVIVAL; CELLS; DNA DAMAGE; HUMANS; ULTRASONOGRAPHY;

EID: 0030442881     PISSN: 03015629     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-5629(96)00089-0     Document Type: Review

References (146)

1. Al-Karma AM, Dinno MA, Stoltz DA, Crum LA, Matthews JC. Calcium and the effects of ultrasound on frog skin. Ultrasound Med Biol 1994;20:73-81.
2. Apfel RE. Acoustic cavitation. Meth Exp Phys 1986;19:355-441.
3. Armour EL, Corry PM. Cytotoxic effects of ultrasound in vitro: dependence on gas content, frequency, radical scavengers, and attachment. Radiat Res 1982;89:369-380.
4. Barnett SB, Baker RSU, Barnstable S. Is pulsed ultrasound mutagenic? In: Lerski RA, Morley P, eds. Ultrasound 82. Proceedings of WFUMB. Oxford: Pergamon:45-48.
5. Barnett SB, Miller MW, Cox C, Carstensen EL. Increased sister chromatid exchanges in Chinese hamster ovary cells exposed to high intensity pulsed ultrasound. Ultrasound Med Biol 1988; 14:397-403.
6. Blackshear PL, Blackshear GL. Mechanical hemolysis. In: Skalak R, Chien S, eds. Handbook of bioengineering. New York: McGraw-Hill, 1987:15.1-15.9.
7. Bleeker HJ, Shung KK, Barnhart JL. Ultrasonic characterization of Albunex , a new contrast agent. J Acoust Soc Am 1987;87:1792-1797.
8. Brauner T, Brummer F, Hulser DF. Histopathology of shock wave treated tumor cell suspensions and multicell tumor spheroids. Ultrasound Med Biol 1989;15:451-460.
9. Brayman AA, Azadniv M, Makin IRS, Miller MW, Carstensen EL, Child SZ, Raeman CH, Meltzer RS, Everbach EC. Effect of Albunex® echo contrast agent on hemolysis of human erythrocytes exposed to high-intensity pulsed ultrasound. Echocardiography 1995;12:13-21.
10. Brayman AA, Azadniv M, Miller MW. Bubble recycling and ultrasonic cell lysis in a stationary exposure vessel. J Acoust Soc Am 1994a;96:627-633.
11. Brayman AA, Azadniv M, Miller MW, Chen X. Bubble recycling and ultrasonic cell lysis in a stationary exposure vessel. J Acoust Soc Am 1994b;96:627-633.
12. Brayman AA, Church CC, Miller MW. Re-evaluation of the concept that high cell concentrations protect cells in vitro from ultrasonically induced lysis. Ultrasound Med Biol 1996;22:497-514.
13. Brayman AA, Doida Y, Miller MW. Apparent contribution of respiratory gas exchange to the in vitro cell density effect in ultrasonic cell lysis. Ultrasound Med Biol 1992;18:701-714.
14. Brayman AA, Miller MW. Bubble cycling and standing waves in ultrasonic cell lysis. Ultrasound Med Biol 1992;18:411-420.
15. Brayman AA, Miller MW. Cell density dependence of the ultrasonic degassing of fixed erythrocyte suspensions. Ultrasound Med Biol 1993;19:243-252.
16. Brayman AA, Miller MW. Ultrasonic cell lysis in vitro upon fractional, discontinuous exposure vessel rotation. J Acoust Soc Am 1994;95:3666-3668.
17. Brummer F, Brenner J, Brauner T, Hulser DF. Effect of shock waves on suspended and immobilized L1210 cells. Ultrasound Med Biol 1989;15:229-239.
18. Carstensen EL, Kelly P, Church CC, Brayman AA, Child SZ, Raeman CH, Schery L. Lysis of erythrocytes by exposure to CW ultrasound. Ultrasound Med Biol 1993;19:147-165.
19. Chapman IV, MacNally NA, Tucker S. Ultrasound-induced changes in rates of influx and efflux of potassium ions in rat thymocytes in vitro. Ultrasound Med Biol 1979;6:47-58.
20. Christenson HK, Claesson PM. Cavitation and the interaction between macroscopic hydrophobic surfaces. Science 1988;239: 390-392.
21. Church CC. A theoretical study of cavitation generated by an extracorporeal shock wave lithotripter. J Acoust Soc Am 1989; 86:215-227.
22. Church CC. Bubble dynamics and bubble-cell interactions induced by an acoustic traveling wave. 1996 (in press).
23. Church CC, Flynn HG, Miller MW, Sacks PG. The exposure vessel as a factor in ultrasonically-induced mammalian cell lysis. II. An explanation of the need to rotate exposure tubes. Ultrasound Med Biol 1982;8:299-309.
24. Church CC, Miller MW. The kinetics and mechanics of ultrasonically-induced cell lysis produced by non-trapped bubbles in a rotating culture tube. Ultrasound Med Biol 1983;9:385-393.
25. Ciaravino V, Brulfert A, Miller MW, Jacobsen-Kram D, Morgan WF. Diagnostic ultrasound and sister chromatid exchanges: failure to reproduce positive results. Science 1985;227:1349-1351.
26. Ciaravino V, Miller MW, Carstensen EL. Sister chromatid exchanges in human lymphocytes exposed in vitro to therapeutic ultrasound. Mutat Res 1986;172: 185-188.
27. Ciaravino V, Flynn HG, Miller MW. Pulsed enhancement of acoustic cavitation: a postulated model, Ultrasound Med Biol 1981a; 7:159-166.
28. Ciaravino V, Miller MW, Carstensen EL. Pressure-mediated reduction of ultrasonically-induced cell lysis. Radiat Res 1981b; 88:209-213.
29. Ciaravino V, Miller MW, Kaufman GE. The effect of 1 MHz ultrasound on the proliferation of synchronized Chinese hamster V-79 cells. Ultrasound Med Biol 1981c;7:175-184.
30. Clarke PR, Hill CR. Physical and chemical aspects of ultrasonic disruption of cells. J Acoust Soc Am 1970;47:649-653.
31. Coleman AJ, Saunders JE. A review of the physcal properties and biological effects of the high amplitude acoustic fields used in extracorporeal lithotripsy. Ultrasonics 1993;31:75-89.
32. Coleman AJ, Saunders JE, Crum LA, Dyson M. Acoustic cavitation generated by an extracorporeal shock wave lithotripter. Ultrasound Med Biol 1987;13:69-76.
33. Coleman AJ, Whitlock M, Leighton T, Saunders JE. The spatial distribution of cavitation induced acoustic emission, sonoluminescence and cell lysis in the field of a shock wave lithotripter. Phys Med Biol 1993;38:1545-1560.
34. Conger AD, Ziskin MC, Wittells H. Ultrasonic effects on mammalian multicellular tumor spheroids. J Clin Ultrasound 1981; 9:167-174.
35. Crum LA. Surface oscillations and jet formation in pulsating air bubbles. J Phys 1979;40:131-134.
36. Crum LA, Roy RA, Dinno MA, Church CC, Apfel RE, Holland CK, Madanshetty SI. Acoustic cavitation produced by microsecond pulses of ultrasound: a discussion of some selected results. J Acoust Soc Am 1992;91:1113-1119.
37. Dinno MA, Crum LA, Wu J. The effect of therapeutic ultrasound on electrophysiological parameters of frog skin. Ultrasound Med Biol 1989;15:461-470.
38. Dinno MA, Dyson M, Young SR, Mortimer AJ, Hart J, Crum LA. The significance of membrane changes in the safe and effective use of therapeutic and diagnostic ultrasound. Phys Med Biol 1989b;34:1543-1552.
39. Dinno MA, Al-Karmi AM, Stoltz DA, Matthews JC, Crum LA. Effect of free radical scavengers on changes in ion conductance during exposure to therapeutic ultrasound. Membr Biochem 1993;10:237-247.
40. Doida Y, Miller MW, Cox C, Church CC. Confirmation of an ultrasound-induced mutation in two in vitro mammalian cell lines. Ultrasound Med Biol 1990;16:699-705.
41. Doida Y, Brayman AA, Miller MW. Ultrasound-induced in vitro cell lysis: node-antinode interactions. J Ultrasound Med 1992a;11:413-417.
42. Doida Y, Brayman AA, Miller MW. Modest enhancement of ultrasound-induced mutations in V79 cells in vitro. Ultrasound Med Biol 1992b; 18:465-469.
43. Dooley DA, Child SZ, Carstensen EL, Miller MW. The effects of continuous wave and pulsed ultrasound on rat thymocytes in vitro. Ultrasound Med Biol 1984;9:379-384.
44. Dooley DA, Sacks PG, Miller MW. Production of thymine base damage in ultrasound exposed EMT6 mouse mammary sarcoma cells. Radiat Res 1984;97:71-86.
45. Dunn F. Cellular inactivation by heat and shear. Radiat Environ Biophys 1985;24:131-139.
46. Ellwart JW, Brettel H, Kober LO. Cell membrane damage by ultrasound at different cell concentrations. Ultrasound Med Biol 1988;14:43-50.
47. Fahnestock M, Rimer VG, Yamawaki RM, Ross P, Edmonds PD. Effects of ultrasound exposure in vitro on neuroblastoma cell membranes. Ultrasound Med Biol 1989;15:133-144.
48. Flynn HG, Church CC. Transient pulsations of small gas bubbles in water. J Acoust Soc Am 1988;84:1863-1876.
49. Fu Y-K, Kaufman GE, Miller JW, Griffiths TD, Lange CS. Modification by cysteamine of ultrasound lethality to Chinese hamster V-79 cells. Radiat Res 1979;80:575-580.
50. Fu Y-K, Miller MW, Lange CS, Griffiths TD, Kaufman GE. Ultrasound lethality to synchronous and asynchronous Chinese hamster V-79 cells. Ultrasound Med Biol 1980;6:39-46.
51. Gambihler S, Delius M. Influence of dissolved and free gases on iodine release and cell killing by shock waves in vitro. Ultrasound Med Biol 1992;18:617-623.
52. Gambihler S, Delius M, Brendel W. Biological effects of shock waves: cell disruption, viability and proliferation of L1210 cells exposed to shock waves in vitro. Ultrasound Med Biol 1990;16:587-594.
53. Gregory WD, Miller MW, Carstensen EL, Cataldo FL, Reddy MM. Non-thermal effects of 2 MHz ultrasound on the growth and cytology of Vicia faba roots. Br J Radiol 1974;47:122-129.
54. Gross DR, Miller DL, Williams AR. A search for ultrasonic cavitation within the canine cardiovascular system. Ultrasound Med Biol 1987;11:85-97.
55. Harrison GH, Balcer-Kubiczek EK. Continuous-wave ultrasound and neoplastic transformation in vitro. Ultrasound Med Biol 1989;15:335-340.
56. Harrison GH, Balcer-Kubiczek EK, Eddy HA. Potentiation of chemotherapy by low-level ultrasound. Int J Radiat Biol 1991; 59:1453-1466.
57. Harvey EN. Biological aspects of ultrasonic waves, a general survey. Biol Bull 1930;59, 306-325.
58. Harvey W, Dyson M, Pond JB, Graham R. The in vitro stimulation of protein synthesis in human fibroblasts by therapeutic levels of ultrasound. In: Kazner E, de Vlieger M, Muller HR, McCready VR, eds. Proceedings of the Second European Congress on Ultrasonics in Medicine. Excerpta Medica International Congress series no. 363. Amsterdam: Excerpta Medica Foundation: 10-21.
59. Hawley SA, Dunn F. UHF acoustic interaction with biological media. Naturwissenschaften 1964;51:555.
60. Holland CK, Apfel RE: Thresholds for transient cavitation produced by pulsed ultrasound in a controlled nuclei environment. J Acoust Soc Am 1990;88:2059-2069.
61. Hill CR, Joshi GP. The significance of cavitation in interpreting the biological effects of ultrasound. In: Proceedings of the Conference on Ultrasonics in Biology and Medicine (UBIOMED-70), Warsaw, Poland, pp. 125-131.
62. Holland CK, Roy RA, Apfel RE. In vitro detection of cavitation induced by a diagnostic ultrasound system. IEEE UFFC 1992;39:95-101.
63. Holmer NG, Johnsson A, Josefsson JO. Effects of ultrasonic irradiation upon Amoeba proteus. Z Naturforsch 1975;28c:607-609.
64. Inoue M, Church CC, Brayman A, Miller MW, Malcuit MS. Confirmation of the protective effect of cysteamine in in vitro ultrasound exposures. Ultrasonics 1989;27:362-369.
65. Kaufman GE. Mutagenicity of ultrasound in cultured mammalian cells. Ultrasound Med Biol 1985;11:497-501.
66. Kaufman GE, Miller MW. Growth retardation in Chinese hamster V-79 cells exposed to 1 MHz ultrasound. Ultrasound Med Biol 1978;4:139-144.
67. Kaufman GE, Miller MW, Griffiths TD, Ciaravino V, Carstensen EL. Lysis and viability of cultured mammalian cells exposed to 1 MHz ultrasound. Ultrasound Med Biol 1977;3:21-25.
68. Kober LO, Ellwart JW, Brettel H. Effect of the pulse length of ultrasound on cell membrane damage in vitro. J Acoust Soc Am 1989;86:6-7.
69. Kondo T, Kano E. Enhancement of hyperthermic cell killing by non-thermal effect of ultrasound. Int J Radiat Biol 1987;51:157-166.
70. Kondo T, Kano E. Effect of free radicals induced by ultrasonic cavitation on cell killing. Int J Radiat Biol 1988;54:475-486.
71. Kondo T, Garrison J, Mitchell JB, Riesz P. Free radical formation and cell lysis induced by ultrasound in the presence of different rare gases. Int J Radiat Biol 1988;54:955-962.
72. Lehmann JF. The biophysical mode of action of biologic and therapeutic ultrasonic reactions. J Acoust Soc Am 1953;25:17-25.
73. Li GC, Hahn GM, Tolmach LJ. Cellular inactivation by ultrasound. Nature 1977;267:163.
74. Liebeskind D, Bases R, Elequin F, Neubort S, Leifer R, Goldberg R, Koenigsberg M. Diagnostic ultrasound: effects on the DNA and growth patterns of animals cells. Radiology 1979a; 131:177-184.
75. Liebeskind D, Bases R, Mendez F, Elequin F, Koenigsberg M. Sister chromatid exchanges in human lymphocytes after exposure to diagnostic ultrasound. Science 1979a;205:1273-1275.
76. Liebeskind D, Padawer J, Wolley R, Bases R. Diagnositc ultrasound: time-lapse and transmission electron microscopic studies of cells insonated in vitro. Br J Cancer 45 (suppl V):176-186.
77. Loch EG, Fischer AB, Kuwert E. Effect of diagnostic and therapeutic intensities of ultrasonics on normal and malignant human cells in vitro. Am J Obstet Gynecol 1971;110:457-460.
78. Loverock P, ter Haar G. Synergism between hyperthermia, ultrasound and gamma irradiation. Ultrasound Med Biol 1991; 17:607-612.
79. Loverock P, ter Haar G, Ormerod MG, Imrie PR. The effect of ultrasound on the cytotoxicity of adriamycin. Br J Radiol 1990;63:542-546.
80. Macintosh IJC, Davey DA. Chromosome aberrations induced by an ultrasonic fetal pulse detector. Br Med J 1970;4:92-93.
81. Martins BI, Raju MR, Hayes TL, Tobias CA. Survival of cultured mammalian cells exposed to ultrasound. Radiat Environ Biophys 1977;14:243-250.
82. Mello Filho AC, Menghini R. In vivo formation of single-strand breaks in DNA by hydrogen peroxide is mediated by the Haber-Weiss reaction. Biochem Biophys Acta 1984;781:56-63.
83. Mihran RT, Barnes FS, Wachtel H. Temporally-specific modification of myelinated axon excitability in vitro following a single ultrasound pulse. Ultrasound Med Biol 1990;16:297-309.
84. Miller DL. A review of the ultrasonic bioeffectiveness of microsonation, gas-body activation, and related cavitation-like phenomena. Ultrasound Med Biol 1987;13, 443-470.
85. Miller DL. The influence of hematocrit on hemolysis by ultrasonically activated gas-filled micropores. Ultrasound Med Biol 1988;14:293-297.
86. Miller DL, Nyborg WL, Whitcomb CC. Platelet aggregation induced by ultrasound under specialized conditions in vitro. Science 1979;205:505-507.
87. Miller DL, Reese JA, Frazier MW. Single strand DNA breaks in human leukocytes induced by ultrasound in vitro. Ultrasound Med Biol 1989;15:765-771.
88. Miller DL, Thomas RM. A comparison of hemolytic and sonochemical activity of ultrasonic cavitation in a rotating tube. Ultrasound Med Biol 1993;19:83-90.
89. Miller DL, Thomas RM. Frequency dependence of cavitation activity in a rotating tube exposure system compared to the mechanical index. J Acoust Soc Am 1993a;93:3475-3480.
90. Miller DL, Thomas RM. Cavitation dosimetry: estimates for single bubbles in a rotating-tube exposure system. Ultrasound Med Biol 1994;20:187-193.
91. Miller DL, Thomas RM. Ultrasound contrast agents nucleate inertial cavitation in vitro. Ultrasound Med Biol 1995;21:1059-1065.
92. Miller DL, Thomas RM, Buschbom RL. Comet Assay reveals DNA strand breaks induced by ultrasonic cavitation in vitro. Ultrasound Med Biol 1995;21:841-848.
93. Miller DL, Thomas RM, Frazier ME. Single strand breaks in CHO cell DNA induced by ultrasonic cavitation in vitro. Ultrasound Med Biol 1991a;17:401-406.
94. Miller DL, Thomas RM, Frazier ME. Ultrasonic cavitation indirectly induces single strand breaks in DNA of viable cells in vitro by the action of residual hydrogen peroxide. Ultrasound Med Biol 1991b;17:729-735.
95. Miller DL, Thomas RM, Williams AR. Mechanisms for hemolysis by ultrasonic cavitation in the rotating exposure system. Ultrasound Med Biol 1991c;17: 171-178.
96. Miller DL, Williams AR. Bubble cycling as an explanation of the promotion of ultrasonic cavitation in a rotating tube exposure system. Ultrasound Med Biol 1989;15:641-648.
97. Miller DL, Williams AR. Nucleation and evolution of ultrasonic cavitation in a rotating exposure chamber. Ultrasound Med Biol 1992;11:407-412.
98. Miller MW. Does ultrasound induce sister chromatid exchanges? Ultrasound Med Biol 1985;11:561-570.
99. Miller MW, Azadniv M, Cox C, Miller WM. Lack of induced increase in sister chromatid exchanges in human lymphocytes exposed to in vivo therapeutic ultrasound. Ultrasound Med Biol 1991;17:81-83.
100. Miller MW, Azadniv M, Pettit SE, Church CC, Carstensen EL, Hoffman D. Sister chromatid exchanges in Chinese hamster ovary cells exposed to high intensity pulsed ultrasound: inability to confirm previous positive results. Ultrasound Med Biol 1989a;15:255-262.
101. Miller MW, Azadniv M, Doida Y, Brayman AA. Effect of a stabilized microbubble contrast agent on CW ultrasound induced red blood lysis in vitro. Echocardiography 1995;12:1-11.
102. Miller MW, Church CC, Brayman AA, Malcuit MS, Boyd RW. An explanation for the decrease in cell lysis in a rotating tube with increasing ultrasound intensity. Ultrasound Med Biol 1989a; 15:67-72.
103. Miller MW, Church CC, Ciaravino V. Time lapse and microscopic examinations of insonated in vitro cells. Ultrasound Med Biol 1995;16:73-79.
104. Mortimer AJ, Dyson M. The effect of therapeutic ultrasound on calcium uptake in fibroblasts. Ultrasound Med Biol 1988; 14:499-506.
105. Morton KI, ter Haar G, Stratford IJ, Hill CR. The role of cavitation in the interaction of ultrasound with V79 Chinese cancer cells in vitro. Br J Cancer 1982;45(suppl V):147-150.
106. National Council on Radiation Protection and Measurements (NCRP). Biological effects of ultrasound: mechanisms and clinical implications. NCRP Report No. 74. Bethesda, MD: NCRP, 1983.
107. National Council on Radiation Protection and Measurements (NCRP). Exposure criteria for medical diagnostic ultrasound: I. Criteria based on thermal mechanisms. NCRP Report No. 113. Bethesda, MD: NCRP, 1992.
108. Nyborg WL, Miller DL. Biological implications of bubble dynamics. Appl Sci Res 1982;38:17-24.
109. Prat F, Chapelon JY, Chauffert B, Ponchon T, Cathignol D. Cytotoxic effects of acoustic cavitation on HT-29 cells and a rat peritoneal carcinomatosis in vitro. Cancer Res 1993;51:3024-3029.
110. Prat F, Chapelon JY, El Fadil FA, Theillere T, Ponchon T, Cathignol D. In vivo effects of cavitation alone or in combination with chemotherapy in a peritoneal carcinomatosis in the rat. Br J Cancer 1993;68:13-17.
111. Prat F, Sibille A, Luccioni C, Pansu D, Chapelon JY, Beaumatin J, Ponchon T, Cathignol D. Increased chemocytotoxicity to colon cancer cells by shock wave-induced cavitation. Gastroenterology 1994;108:937-944.
112. Prise KM, Davies S, Michael BD. Cell killing and DNA damage in Chinese hamster V79 cells treated with hydrogen peroxide. Int J Radiat Biol 1989;55:583-592.
113. Prohaska SS, Rimer VG, Tuse D, Pryor GT, Edmonds PD. Conservation of bactericidal activity in ultrasound-exposed murine peritoneal phagocytic cells. Ultrasound Med Biol 1992a;18:601-606.
114. Prohaska SS, Rimer VG, Winters MA, Humphries RC, Tuse D, Edmonds PD Conservation of receptor expression and phagocytic activity of murine macrophages exposed to various ultrasonic regimens in vitro. J Ultrasound Med 1992b;11:93-101.
115. Randazzo RF, Chaussy CG, Fuchs GJ, Bhuta SM, Lovrekovich H, deKernion JB. The in vitro and in vivo effects of extracorporeal shock waves on malignant cells. Urol Res 1988;16:419-426.
116. Riesz P, Kondo T. Free radical formation induced by ultrasound and its biological implications. Free Rad Biol Med 1992;13:247-270.
117. Saad AH. Some biological effects of ultrasound. PhD thesis, University of Manchester, Manchester, UK.
118. Saad AH, Hahn GM. Ultrasound enhanced drug toxicity on Chinese hamster ovary cells in vitro. Cancer Res 1989;49:5931-5934.
119. Saad AH, Williams AR. Possible mechanisms for the agitation-induced enhancement of acoustic cavitation in vitro. J Acoust Soc Am 1985;78:429-434.
120. Sacks PG, Miller MW, Church CC. The exposure vessel as a factor in ultrasonically induced mammalian cell lysis: a comparison of tube and chamber systems. Ultrasound Med Biol 1983;8:289-298.
121. Sacks PG, Miller MW, Sutherland RM. Response of multicell spheroids to 1 MHz ultrasonic irradiation: cavitation related damage. Radiat Res 1983;93:545-559.
122. Shima A, Takayama K, Tomita Y. Mechanisms of impact pressure generation from spark-generated bubble collapse near a wall. A1AA J 1983;21:55-59.
123. Smits GA, Oosterhof GON, deRuyter AE, Schalken JA, Debruyne FMJ. Cytotoxic effects of high energy shock waves in different in vitro models: influence of the experimental set-up. J Urol 1991;145:171-175.
124. Stella M, Trevison L, Montaldi A, Azccaria G, Rossi G, Bianchi V, Levis AG. Induction of sister-chromatid exchanges in human lymphocytes exposed in vitro and in vivo to therapeutic ultrasound. Mutat Res 1984;138:75-85.
125. Steinbach P, Hofstadter F, Nicolai H, Rossler W, Wieland W. In vitro investigations on cellular damage induced by high energy shock waves. Ultrasound Med Biol 1992;18:691-699.
126. Suhr D, Brummer F, Irmer U, Schlachter M, Hulser DF. Reduced cavitation-induced cellular damage by the antioxidative effect of vitamin E. Ultrasonics 1994;32:301-308.
127. ter Haar GR, Stratford IT, Hill CR. Ultrasonic irradiation of mammalian cells in vitro at hyperthermic temperatures. Br J Radiol 1980;53:784-789.
128. ter Haar GR, Walling J, Loverock P, Townsend S. The effect of combined heat and ultrasound on multicellular tumour spheroids. Int J Radiat Biol 1988;53:813-827.
129. Thacker J. Investigations into genetic and inherited changes produced by ultrasound. In: Nyborg WL, Ziskin MC, eds. Biological effects of ultrasound. New York: Churchill Livingstone, 1985:67-76.
130. Tomita Y, Shima A. Mechanisms of impulsive pressure generation and damage pit formation by bubble collapse. J Fluid Mech 1986;164:535-564.
131. Umemura S, Yumita N, Nishigaki R, Umemura K. Mechanism of cell damage by ultrasound in combination with hematoporphyrin. Jpn J Cancer Res 1990;81:962-966.
132. Veress E, Vincze J. The haemolysing action of ultrasound on erythrocytes. Acustica 1977;36:100-103.
133. Verall RE, Sehgal CM. Sonoluminescence. In: Suslick KS, ed. Ultrasound. Its chemical, physical and biological effects. New York: VCH 1988:227-286.
134. Vogel A, Lauterborn W. Acoustic transient generation by laser-generated cavitation bubbles near solid boundaries. J Acoust Soc Am 1988;84:719-731.
135. Vona DF, Miller MW, Maillie HD, Raeman CH. A test of the hypothesis that cavitation at the focal area of an extracorporeal shock wave lithotripter produces far ultraviolet and soft X-ray emissions. J Acoust Soc Am 1995;98:706-711.
136. Wagai T, Kikuchi Y. Destruction of transplantable ascites tumors by means of intense ultrasound. In: Kelly E, ed. Ultrasonic energy. Urbana, IL: University of Illinois Press, 1975:179-189.
137. Watmough DJ, Lakshimi R, Ghezzi F, Quan KM, Watmough JA, Khizhryak E, Pashovkin TN, Sarvazyan AP. The effect of gas bubbles on the production of ultrasound hypothermia at 0.75 MHz: a phantom study. Ultrasound Med Biol 1993;19:231-241.
138. Watmough DJ, Quan KM, Shiran MB. Possible explanation for the unexpected absence of gross biological damage to membranes of cells insonated in suspension and in surface culture in chambers exposed to standing and progressive wave fields. Ultrasonics 1990;28:142-148.
139. Wegner R-D, Lang R. Absence of a mutagenic effect of diagnostic ultrasound in the Salmonella mutagenicity test (Ames Test). IEEE UFFC 1986;33:171-178.
140. Williams AR. A possible alteration in the permeability of ascites cell membranes after exposure to acoustic microstreaming. J Cell Sci 1973;12:875-885.
141. Williams AR. Absence of meaningful thresholds for bioeffect studies on cell suspensions in vitro. Br J Cancer 1982;45(suppl):192-195.
142. Williams AR, Kubowicz G, Cramer E, Schlief R. The effects of the microbubble suspension SH U 454 (Echovist®) on ultrasonically-induced cell lysis in a rotating tube exposure system. Echocardiography 1991;8:423-433.
143. Williams AR, Miller DL. The role of non-acoustic factors in the induction and proliferation of cavitational activity in vitro. Phys Med Biol 1989;34:1561-1569.
144. Young SR, Dyson M. Macrophage responsiveness to therapeutic ultrasound. Ultrasound Med Biol 1989;16:809-816.
145. Yumita N, Nishigaki R, Umemura K, Umemura S. Synergistic effect of ultrasound and hematoporphyrin on sarcoma 180. Jpn J Cancer Res 1991;81:304-308.
146. Zhu WH, Miller MW, Cox C. Lack of increase in cell transformation frequency of C3H cells after exposure to pulsed ultrasound. Ultrasonics 1991;29:81-84.