Histological and Biochemical Analysis of Mechanical and Thermal Bioeffects in Boiling Histotripsy Lesions Induced by High Intensity Focused Ultrasound

Ultrasound in Medicine and Biology

Volumn 39, Issue 3, 2013, Pages 424-438

  Wang, Yak Nam ^a   Khokhlova, Tatiana ^b   Bailey, Michael ^a   Hwang, Joo Ha ^a,b   Khokhlova, Vera ^c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Boiling; HIFU; High intensity focused ultrasound; Histology; Histotripsy; Lesion; Protein analysis; Thermal effects

Indexed keywords

AMIDES; BOILING LIQUIDS; DENATURATION; EMULSIFICATION; HISTOLOGY; PROTEINS; THERMAL EFFECTS; TISSUE; ULTRASONIC TESTING;

HIFU; HIGH INTENSITY FOCUSED ULTRASOUND; HISTOTRIPSY; LESION; PROTEIN ANALYSIS;

PHASE TRANSITIONS;

EOSIN;

ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BOILING HISTOTRIPSY; CELL NUCLEUS; CELL STRUCTURE; CELL VACUOLE; CONTROLLED STUDY; DENATURATION; ENZYME ACTIVITY; EX VIVO STUDY; HEAT TRANSFER; HIGH INTENSITY FOCUSED ULTRASOUND; HISTOLOGY; LONGITUDINAL STUDY; MEMBRANE DAMAGE; NON INVASIVE PROCEDURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; THERMAL INJURY; TISSUE HOMOGENATE; TISSUE PREPARATION;

EID: 84873523527     PISSN: 03015629     EISSN: 1879291X     Source Type: Journal    
DOI: 10.1016/j.ultrasmedbio.2012.10.012     Document Type: Article

References (34)

1. Bharat S., Techavipoo U., Kiss M.Z., Liu W., Varghese T. Monitoring stiffness changes in lesions after radiofrequency ablation at different temperatures and durations of ablation. Ultrasound Med Biol 2005, 31:415-422.
2. Canney M., Khokhlova V., Bailey M., Sapozhnikov O., Crum L. Acoustic characterization of high intensity focused ultrasound fields: A combined measurement and modeling approach. J Acoust Soc Am 2008, 124:2406-2420.
3. Canney M., Khokhlova V., Bessonova O., Bailey M., Crum L. Shock-induced heating and millisecond boiling in gels and tissue due to high intensity focused ultrasound. Ultrasound Med Biol 2010, 36:250-267.
4. Canney M., Khokhlova V., Hwang J.H., Khokhlova T., Bailey M., Crum L. Tissue erosion using shock wave heating and millisecond boiling in high intensity ultrasound field. Proceedings of the Ninth International Symposium on Therapeutic Ultrasound 2009, AIP Conference Proceedings, Melville, NY, 36-39.
5. Date R.S., Biggins J., Paterson I., Denton J., McMahon R.F., Siriwardena A.K. Development and validation of an experimental model for the assessment of radiofrequency ablation of pancreatic parenchyma. Pancreas 2005, 30:266-271.
6. Dubinsky T.J., Cuevas C., Dighe M.K., Kolokythas O., Hwang J.H. High-intensity focused ultrasound: Current potential and oncologic applications. AJR Am J Roentgenol 2008, 190:191-199.
7. Duck F. Physical properties of tissue: a comprehensive reference book 1990, Academic Press Limited, London, pp. 9-137.
8. Hamilton M., Blackstock D. Nonlinear acoustics 1998, Academic Press, London, p. 284.
9. Jung S.E., Cho S.H., Jang J.H., Han J.Y. High-intensity focused ultrasound ablation in hepatic and pancreatic cancer: Complications. Abdom Imaging 2011, 36:185-195.
10. Khokhlova T., Canney M., Lee D., Marro K., Crum L., Khokhlova V., Bailey M. Magnetic resonance imaging of boiling induced by high intensity focused ultrasound. J Acoust Soc Am 2009, 125:2420-2431.
11. Khokhlova T.D., Canney M.S., Khokhlova V.A., Sapozhnikov O.A., Crum L.A., Bailey M.R. Controlled tissue emulsification produced by high intensity focused ultrasound shock waves and millisecond boiling. J Acoust Soc Am 2011, 130:3498-3510.
12. Khokhlova T.D., Simon J.C., Wang Y.N., Paun M., Starr F.L., Khokhlova V.A., Crum L.A., Hwang J.H., Kaczkowski P.J., Bailey M.R. In vivo tissue emulsification using millisecond boiling induced by high intensity focused ultrasound. J Acoust Soc Am 2011, 129:2477.
13. Khokhlova VA, Yuldashev PV, Bobkova SM, Ilyin SA. The role of nonlinear propagation effects in ablation of soft tissue behind the rib cage using a HIFU phased array. Eleventh International Symposium on Therapeutic Ultrasound. New York: April 2011c, p. 52.
14. Kim Y., Wang T.-Y., Xu Zhen, Cain C.A. Lesion generation through ribs using histotripsy therapy without aberration correction. IEEE Trans Ultrason Ferroelectr Freq Control 2011, 58:2334-2343.
15. Klingler H.C., Susani M., Seip R., Mauermann J., Sanghvi N., Marberger M.J. A novel approach to energy ablative therapy of small renal tumours: Laparoscopic high-intensity focused ultrasound. Eur Urol 2008, 53:810-818.
16. Lake A.M., Hall T.M., Kieran K., Fowlkes J.B., Cain C.A., Roberts W.W. Histotripsy: Minimally invasive technology for prostatic tissue ablation in an in vivo canine model. Urology 2008, 72:682-686.
17. Lam F.T., Mavor A.I.D., Potts D.J., Giles G.R. Improved 72-hour renal preservation with phosphate-buffered sucrose. Transplantation 1989, 47:767-771.
18. Maxwell A.D., Wang T.-Y., Cain C.A., Fowlkes J.B., Sapozhnikov O.A., Bailey M.R., Xu Z. Cavitation clouds created by shock scattering from bubbles during histotripsy. J Acoust Soc Am 2011, 130:1888-1898.
19. Miller D.L., Smith N.B., Bailey M.R., Czarnota G.J., Hynynen K., Makin I.S. Overview of therapeutic ultrasound applications and safety considerations. J Ultrasound Med 2012, 31:623-634.
20. Novikoff A.B., Shin W.Y., Drucker J. Mitochondrial localization of oxidative enzymes: Staining results with two tetrazolium salts. J Biophys Biochem Cytol 1961, 9:47-61.
21. Bessonova O.V., Khokhlova V.A., Canney M.S., Bailey M.R., Crum L.A. A derating method for therapeutic applications of high intensity focused ultrasound. Acoust Phys 2010, 56:376-385.
22. Owens G.E., Miller R.M., Owens S.T., Swanson S.D., Ives K., Ensing G., Gordon D., Xu Z. Intermediate-term effects of intracardiac communications created noninvasively by therapeutic ultrasound (histotripsy) in a porcine model. Pediatr Cardiol 2012, 33:83-89.
23. Parmentier H., Melodelima D., N'Djin A., Chesnais S., Chapelon J.Y., Rivoire M. High-intensity focused ultrasound ablation for the treatment of colorectal liver metastases during an open procedure study on the pig. Ann Surg 2009, 249:129-136.
24. Parsons J., Cain C., Abrams G., Fowlkes J. Pulsed cavitational ultrasound therapy for controlled tissue homogenization. Ultrasound Med Biol 2006, 32:115-129.
25. Pohlhammer J., O'Brien W.D. Dependence of the ultrasonic scatter coefficient on collagen concentration in mammalian tissues. J Acoust Soc Am 1981, 69:283-285.
26. Raccosta S., Manno M., Bulone D., Giacomazza D., Militello V., Martorana V., San Biagio P.L. Irreversible gelation of thermally unfolded proteins: structural and mechanical properties of lysozyme aggregates. Eur Biophys J 2010, 39:1007-1017.
27. Roberts W.W., Hall T.L., Ives K., Wolf J.S., Fowlkes J.B., Cain C.A. Pulsed cavitational ultrasound: A noninvasive technology for controlled tissue ablation (histotripsy) in the rabbit kidney. J Urol 2006, 175:734-738.
28. Physical principles of ultrasonic technology, volume 2 1973, 4-88. Plenum Press, New York. L. Rozenberg (Ed.).
29. Sapareto S., Dewey W. Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys 1984, 10:787-800.
30. Simon J., Sapozhnikov O.A., Khokhlova V.A., Khokhlova T.D., Bailey M.R., Crum L.A. Miniature acoustic fountain as a possible mechanism for tissue emulsification during millisecond boiling in HIFU fields. J Acoust Soc Am 2011, 129:2478.
31. ter Haar G. Ultrasound focal beam surgery. Ultrasound Med Biol 1995, 21:1089-1100.
32. Winterroth F., Xu Z., Wang T.-Y., Wilkinson J.E., Fowlkes J.B., Roberts W.W., Cain C.A. Examining and analyzing subcellular morphology of renal tissue treated by histotripsy. Ultrasound Med Biol 2011, 37:78-86.
33. Wu F., Wang Z.-B., Cao Y.-D., Xu Z.-L., Zhou Q., Zhu H., Chen W- Z. Heat fixation of cancer cells ablated with high-intensity-focused ultrasound in patients with breast cancer. Am J Surg 2006, 192:179-184.
34. Zayas J.F. Functionality of proteins in food 1997, Springer, Berlin, pp. 6-75.