A generalized Rayleigh–Plesset-type bubble dynamics model with a damage mechanism is developed for cavitation and damage of soft materials by focused ultrasound bursts. This study is linked to recent experimental observations in tissue-mimicking polyacrylamide and agar gel phantoms subjected to bursts of a kind being considered specifically for lithotripsy. These show bubble activation at multiple sites during the initial pulses. More cavities appear continuously through the course of the observations, similar to what is deduced in pig kidney tissues in shock-wave lithotripsy. Two different material models are used to represent the distinct properties of the two gel materials. The polyacrylamide gel is represented with a neo-Hookean elastic model and damaged based upon a maximum-strain criterion; the agar gel is represented with a strain-hardening Fung model and damaged according to the strain-energy-based Griffith's fracture criterion. Estimates based upon independently determined elasticity and viscosity of the two gel materials suggest that bubble confinement should be sufficient to prevent damage in the gels, and presumably injury in some tissues. Damage accumulation is therefore proposed to occur via a material fatigue, which is shown to be consistent with observed delays in widespread cavitation activity.

1.
A. P.
Evan
,
L. R.
Willis
,
J. A.
McAteer
,
M. R.
Bailey
,
B. A.
Connors
,
Y.
Shao
,
J. E.
Lingeman
,
J. C.
Williams
,
N. S.
Fineberg
, and
L. A.
Crum
, “
Kidney damage and renal functional changes are minimized by waveform control that suppresses cavitation in shock wave lithotripsy
,”
J. Urol.
168
,
1556
1562
(
2002
).
2.
B. R.
Matlaga
,
J. A.
McAteer
,
B. A.
Connors
,
R. K.
Handa
,
A. P.
Evan
,
J. C.
Williams
,
J. E.
Lingeman
, and
L. R.
Willis
, “
Potential for cavitation-mediated tissue damage in shockwave lithotripsy
,”
J. Endourol.
22
,
121
126
(
2008
).
3.
W.
Kreider
,
A. D.
Maxwell
,
B. W.
Cunitz
,
Y.
Wang
,
D.
Lee
,
M. D.
Sorensen
,
J. D.
Harper
,
O. A.
Sapozhnikov
,
V. A.
Khokhlova
, and
M. R.
Bailey
, “
In vivo cavitation thresholds and injury observations related to burst wave lithotripsy
,”
J. Acoust. Soc. Am.
138
,
1846
1846
(
2015
).
4.
A. P.
Evan
and
J. A.
McAteer
, “
Q-effects of shock wave lithotripsy
,” in
Kidney Stones: Medical and Surgical Management
(
Lippincott-Raven
,
Philadelphia, NY
,
1996
), pp.
549
570
.
5.
Y.
Shao
,
B. A.
Connors
,
A. P.
Evan
,
L. R.
Willis
,
D. A.
Lifshitz
, and
J. E.
Lingeman
, “
Morphological changes induced in the pig kidney by extracorporeal shock wave lithotripsy: Nephron injury
,”
Anat. Rec. A Discov. Mol. Cell. Evol. Biol.
275
,
979
989
(
2003
).
6.
M. R.
Bailey
,
Y. A.
Pishchalnikov
,
O. A.
Sapozhnikov
,
R. O.
Cleveland
,
J. A.
McAteer
,
N. A.
Miller
,
I. V.
Pishchalnikova
,
B. A.
Connors
,
L. A.
Crum
, and
A. P.
Evan
, “
Cavitation detection during shock-wave lithotripsy
,”
Ultrasound Med. Biol.
31
,
1245
1256
(
2005
).
7.
T. G.
Leighton
,
F.
Fedele
,
A. J.
Coleman
,
C.
McCarthy
,
S.
Ryves
,
A. M.
Hurrell
,
A.
De Stefano
, and
P. R.
White
, “
A passive acoustic device for real-time monitoring of the efficacy of shockwave lithotripsy treatment
,”
Ultrasound Med. Biol.
34
,
1651
1665
(
2008
).
8.
A. D.
Maxwell
,
B. W.
Cunitz
,
W.
Kreider
,
O. A.
Sapozhnikov
,
R. S.
Hsi
,
J. D.
Harper
,
M. R.
Bailey
, and
M. D.
Sorensen
, “
Fragmentation of urinary calculi in vitro by burst wave lithotripsy
,”
J. Urol.
193
,
338
344
(
2015
).
9.
W.
Kreider
,
A. D.
Maxwell
,
B. W.
Cunitz
,
Y.-N.
Wang
,
D.
Lee
,
K.
Maeda
,
P.
Movahed
,
V. A.
Khokhlova
,
M. R.
Bailey
,
T.
Colonius
, and
J.
Freund
, “
Ultrasound imaging feedback to control kidney injury caused by burst wave lithotripsy
,” in
33rd World Congress of Endourology & SWL
, London, UK,
2015
.
10.
Y.-N.
Wang
,
W.
Kreider
,
A.
Maxwell
,
D.
Lee
,
J.
Park
,
B.
Cunitz
,
M.
Sorensen
,
R.
Handa
,
M.
Bailey
, and
V.
Khokhlova
, “
The use of Magnetic Resonance Imaging to evaluate injury caused by burst wave lithotripsy for stone comminution
,” in
33rd World Congress of Endourology & SWL
, London, UK,
2015
.
11.
W. W.
Roberts
,
T. L.
Hall
,
K.
Ives
,
J. S.
Wolf
,
J. B.
Fowlkes
, and
C. A.
Cain
, “
Pulsed cavitational ultrasound: A noninvasive technology for controlled tissue ablation (histotripsy) in the rabbit kidney
,”
J. Urol.
175
,
734
738
(
2006
).
12.
Z.
Xu
,
J. B.
Fowlkes
,
A.
Ludomirsky
, and
C. A.
Cain
, “
Investigation of intensity thresholds for ultrasound tissue erosion
,”
Ultrasound Med. Biol.
31
,
1673
1682
(
2005
).
13.
Y. N.
Wang
,
T.
Khokhlova
,
M.
Bailey
,
J. H.
Hwang
, and
V.
Khokhlova
, “
Histological and biochemical analysis of mechanical and thermal bioeffects in boiling histotripsy lesions induced by high intensity focused ultrasound
,”
Ultrasound Med. Biol.
39
(
3
),
424
438
(
2013
).
14.
V. A.
Khokhlova
,
J. B.
Fowlkes
,
W. W.
Roberts
,
G. R.
Schade
,
Z.
Xu
,
T. D.
Khokhlova
,
T. L.
Hall
,
A. D.
Maxwell
,
Y. N.
Wang
, and
C. A.
Cain
, “
Histotripsy methods in mechanical disintegration of tissue: Towards clinical applications
,”
Int. J. Hyperthermia
31
(
2
),
145
162
(
2015
).
15.
M. S.
Plesset
, “
The dynamics of cavitation bubbles
,”
J. Appl. Mech.
16
,
277
282
(
1949
).
16.
J. W. S.
Rayleigh
, “
On the pressure developed in a liquid during the collapse of a spherical cavity
,”
Philos. Mag.
34
,
94
98
(
1917
).
17.
M. S.
Plesset
and
A.
Prosperetti
, “
Bubble dynamics and cavitation
,”
Ann. Rev. Fluid Mech.
9
,
145
185
(
1977
).
18.
C. E.
Brennen
,
Cavitation and Bubble Dynamics
(
Oxford University Press
,
New York
,
1995
), p.
286
.
19.
F. R.
Gilmore
, “
The growth or collapse of a spherical bubble in a viscous compressible liquid
,”
Report No. 26-4
,
1952
.
20.
J. B.
Keller
and
M.
Miksis
, “
Bubble oscillations of large amplitude
,”
J. Acoust. Soc. Am.
68
,
628
633
(
1980
).
21.
A.
Prosperetti
and
A.
Lezzi
, “
Bubble dynamics in a compressible liquid. Part 1. First-order theory
,”
J. Fluid Mech.
168
,
457
478
(
1986
).
22.
J. S.
Allen
,
R.
Roy
, and
C. C.
Church
, “
On the role of shear viscosity in mediating inertial cavitation from short–pulse, megahertz-frequency ultrasound
,”
IEEE Trans. Ultrason. Ferroelectr. Freq. Control
44
,
743
751
(
1997
).
23.
J. S.
Allen
and
R. A.
Roy
, “
Dynamics of gas bubbles in viscoelastic fluids. I. Linear viscoelasticity
,”
J. Acoust. Soc. Am.
107
,
3167
3178
(
2000
).
24.
J. B.
Freund
, “
Suppression of shocked-bubble expansion due to tissue confinement with application to shock-wave lithotripsy
,”
J. Acoust. Soc. Am.
123
,
2867
2874
(
2008
).
25.
A. D.
Maxwell
,
C. A.
Cain
,
T. L.
Hall
,
J. B.
Fowlkes
, and
Z.
Xu
, “
Probability of cavitation for single ultrasound pulses applied to tissues and tissue-mimicking materials
,”
Ultrasound Med. Biol.
39
,
449
465
(
2013
).
26.
E.
Vlaisavljevich
,
A.
Maxwell
,
M.
Warnez
,
E.
Johnsen
,
C.
Cain
, and
Z.
Xu
, “
Histotripsy-induced cavitation cloud initiation thresholds in tissues of different mechanical properties
,”
IEEE Trans. Ultrason. Ferroelectr. Freq. Control
61
,
341
352
(
2014
).
27.
X.
Yang
and
C. C.
Church
, “
A model for the dynamics of gas bubbles in soft tissue
,”
J. Acoust. Soc. Am.
118
,
3595
3606
(
2005
).
28.
R.
Gaudron
,
M. T.
Warnez
, and
E.
Johnsen
, “
Bubble dynamics in a viscoelastic medium with nonlinear elasticity
,”
J. Fluid Mech.
766
,
54
75
(
2015
).
29.
J.
Diani
, “
Irreversible growth of a spherical cavity in rubber-like material: A fracture mechanics description
,”
Int. J. Fracture
112
,
151
161
(
2001
).
30.
A. N.
Gent
and
C.
Wang
, “
Fracture mechanics and cavitation in rubber-like solids
,”
J. Mater. Sci.
26
,
3392
3395
(
1991
).
31.
P.
Movahed
,
W.
Kreider
,
A. D.
Maxwell
,
M. R.
Bailey
, and
J. B.
Freund
, “
Ultrasound induced bubble clusters and tunnels in tissue-mimicking agarose phantoms
,” (unpublished) (
2016
).
32.
F.
Hamaguchi
and
K.
Ando
, “
Linear oscillation of gas bubbles in a viscoelastic material under ultrasound irradiation
,”
Phys. Fluids
27
(
11
),
113103
(
2015
).
33.
S.
Catheline
,
J.-L.
Gennisson
,
G.
Delon
,
M.
Fink
,
R.
Sinkus
,
S.
Abouelkaram
, and
J.
Culioli
, “
Measurement of viscoelastic properties of homogeneous soft solid using transient elastography: An inverse problem approach
,”
J. Acoust. Soc. Am.
116
,
3734
3741
(
2004
).
34.
L.
Liu
,
Y.
Fan
, and
W.
Li
, “
Viscoelastic shock wave in ballistic gelatin behind soft body armor
,”
J. Mech. Behav. Biomed. Mater.
34
,
199
207
(
2014
).
35.
V. T.
Nayar
,
J. D.
Weiland
,
C. S.
Nelson
, and
A. M.
Hodge
, “
Elastic and viscoelastic characterization of agar
,”
J. Mech. Behav. Biomed. Mater.
7
,
60
68
(
2012
).
36.
J.
Zhang
,
C. R.
Daubert
, and
E. A.
Foegeding
, “
Characterization of polyacrylamide gels as an elastic model for food gels
,”
Rheol. Acta
44
,
622
630
(
2005
).
37.
S. J.
Lind
and
T. N.
Phillips
, “
Bubble collapse in compressible fluids using a spectral element marker particle method. Part 2. Viscoelastic fluids
,”
Int. J. Numer. Methods Fluids
71
(
9
),
1103
1130
(
2013
).
38.
C.
Hua
and
E.
Johnsen
, “
Nonlinear oscillations following the Rayleigh collapse of a gas bubble in a linear viscoelastic (tissue-like) medium
,”
Phys. Fluids
25
(
8
),
083101
(
2013
).
39.
K.
Foteinopoulou
and
M.
Laso
, “
Numerical simulation of bubble dynamics in a Phan-Thien–Tanner liquid: Non-linear shape and size oscillatory response under periodic pressure
,”
Ultrasonics
50
,
758
776
(
2010
).
40.
M. T.
Warnez
and
E.
Johnsen
, “
Numerical modeling of bubble dynamics in viscoelastic media with relaxation
,”
Phys. Fluids
27
(
6
),
063103
(
2015
).
41.
A. P.
Evan
,
L. R.
Willis
,
J. E.
Lingeman
, and
J. A.
McAteer
, “
Renal trauma and the risk of long-term complications in shock wave lithotripsy
,”
Nephron
78
,
1
8
(
1998
).
42.
A. F.
Bower
,
Applied Mechanics of Solids
(
CRC Press
, Boca Raton,
FL
,
2009
),
p. 775
.
43.
Y. C.
Fung
,
Biomechanics: Mechanical Properties of Living Tissues
(
Springer
Science & Business Media,
New York
,
2013
.
44.
Y. C.
Fung
,
K.
Fronek
, and
P.
Patitucci
, “
Pseudoelasticity of arteries and the choice of its mathematical expression
,”
Am. J. Physiol. Heart Circ. Physiol.
237
,
620
631
(
1979
).
45.
G. B.
Arfken
,
H. J.
Weber
, and
F. E.
Harris
,
Mathematical Method for Physicists: A Comprehensive Guide
(
Academic
,
Oxford
,
2013
),
p.1220
.
46.
A.
Prosperetti
, “
A generalization of the Rayleigh–Plesset equation of bubble dynamics
,”
Phys. Fluids
25
,
409
410
(
1982
).
47.
M. A.
Ainslie
and
T. G.
Leighton
, “
Review of scattering and extinction cross-sections, damping factors, and resonance frequencies of a spherical gas bubble
,”
J. Acoust. Soc. Am.
130
,
3184
3208
(
2011
).
48.
A. N.
Gent
and
P. B.
Lindley
, “
Internal rupture of bonded rubber cylinders in tension
,”
Proc. R. Soc. A
249
,
195
205
(
1959
).
49.
V.
Lefevre
,
K.
Ravi-Chandar
, and
O.
Lopez-Pamies
, “
Cavitation in rubber: An elastic instability or a fracture phenomenon?,”
Int. J. Fracture
192
,
1
23
(
2014
).
50.
A.
Eller
and
H. G.
Flynn
, “
Rectified diffusion during nonlinear pulsations of cavitation bubbles
,”
J. Acoust. Soc. Am.
37
,
493
503
(
1965
).
51.
L. A.
Crum
,
S.
Daniels
,
G. R.
Ter Haar
, and
M.
Dyson
, “
Ultrasonically induced gas bubble production in agar based gels: Part II, theoretical analysis
,”
Ultrasound Med. Biol.
13
(
9
),
541
554
(
1987
).
52.
P. S.
Epstein
and
M. S.
Plesset
, “
On the stability of gas bubbles in liquid–gas solutions
,”
J. Chem. Phys.
18
,
1505
1509
(
1950
).
53.
A.
Chakrabarti
and
M. K.
Chaudhury
, “
Direct measurement of the surface tension of a soft elastic hydrogel: Exploration of elastocapillary instability in adhesion
,”
Langmuir
29
,
6926
6935
(
2013
).
54.
W.
Press
,
S.
Teukolsky
,
W.
Vetterling
, and
B.
Flannery
,
Numerical Recipes in Fortran 77: The Art of Scientific Computing
(
Cambridge University Press
,
New York
,
1992
), p.
933
.
55.
I.
Choi
and
R. T.
Shield
, “
Second-order effects in problems for a class of elastic materials
,”
Z. Angew. Math. Phys.
32
,
361
381
(
1981
).
56.
L. M.
Barrangou
,
C. R.
Daubert
, and
E. A.
Foegeding
, “
Textural properties of agarose gels. I. Rheological and fracture properties
,”
Food Hydrocoll.
20
,
184
195
(
2006
).
57.
D. T. N.
Chen
,
Q.
Wen
,
P. A.
Janmey
,
J. C.
Crocker
, and
A. G.
Yodh
, “
Rheology of soft materials
,”
Annu. Rev. Condens. Matter Phys.
1
,
301
322
(
2010
).
58.
A.
Livne
,
E.
Bouchbinder
,
I.
Svetlizky
, and
J.
Fineberg
, “
The near-tip fields of fast cracks
,”
Science
327
(
5971
),
1359
1363
(
2010
).
59.
T. C.
Laurent
, “
Determination of the structure of agarose gels by gel chromatography
,”
BBA-Gen. Subjects
136
,
199
205
(
1967
).
60.
R. B.
Bird
,
R. C.
Armstrong
,
O.
Hassager
, and
C. F.
Curtiss
,
Dynamics of Polymeric Liquids
(
Wiley
,
New York
,
1977
), Vol. 2, p.
421
.
61.
O.
Ishizuka
and
K.
Koyama
, “
Elongational viscosity at a constant elongational strain rate of polypropylene melt
,”
Polymer
21
,
164
170
(
1980
).
62.
A. A.
Griffith
, “
The phenomena of rupture and flow in solids
,”
Philos. Trans. R. Soc. A
221
,
582
593
(
1921
).
63.
S. B.
Hutchens
,
S.
Fakhouri
, and
A. J.
Crosby
, “
Elastic cavitation and fracture via injection
,”
Soft Matter
12
(
9
),
2557
2566
(
2016
).
64.
H. J.
Kwon
,
A. D.
Rogalsky
, and
D.
Kim
, “
On the measurement of fracture toughness of soft biogel
,”
Polym. Eng. Sci.
51
,
1078
1086
(
2011
).
65.
E. A.
Foegeding
,
C.
Gonzalez
,
D. D.
Hamann
, and
S.
Case
, “
Polyacrylamide gels as elastic models for food gels
,”
Food Hydrocoll.
8
,
125
134
(
1994
).
66.
J. Y.
Sun
,
X.
Zhao
,
W. R. K.
Illeperuma
,
O.
Chaudhuri
,
K. H.
Oh
,
D. J.
Mooney
,
J. J.
Vlassak
, and
Z.
Suo
, “
Highly stretchable and tough hydrogels
,”
Nature
489
,
133
136
(
2012
).
67.
S.
Kundu
and
A. J.
Crosby
, “
Cavitation and fracture behavior of polyacrylamide hydrogels
,”
Soft Matter
5
,
3963
3968
(
2009
).
68.
M. A.
Miner
, “
Cumulative damage in fatigue
,”
J. Appl. Mech.
12
,
159
164
(
1945
).
69.
N. E.
Dowling
,
Mechanical Behavior of Materials: Engineering Methods for Deformation, Fracture, and Fatigue
(
Prentice Hall
,
Upper Saddle River, NJ
,
1993
).
70.
V. A. P.
Martins dos Santos
,
E. J. T. M.
Leenen
,
M. M.
Rippoll
,
C.
van der Sluis
,
T.
van Vliet
,
J.
Tramper
, and
R. H.
Wijffels
, “
Relevance of rheological properties of gel beads for their mechanical stability in bioreactors
,”
Biotechnol. Bioeng.
56
,
517
529
(
1997
).
71.
S. H.
Teoh
, “
Fatigue of biomaterials: A review
,”
Int. J. Fatigue
22
,
825
837
(
2000
).
72.
R. W.
Hertzberg
and
J. A.
Manson
,
Fatigue of Engineering Plastics
(
Academic
,
New York
,
1980
), p.
295
.
73.
D. J.
Krzypow
and
C. M.
Rimnac
, “
Cyclic steady state stress–strain behavior of UHMW polyethylene
,”
Biomaterials
21
,
2081
2087
(
2000
).
74.
R. W.
Meyer
and
L. A.
Pruitt
, “
The effect of cyclic true strain on the morphology, structure, and relaxation behavior of ultra high molecular weight polyethylene
,”
Polymer
42
,
5293
5306
(
2001
).
75.
H.
Schechtman
and
D. L.
Bader
, “
Fatigue damage of human tendons
,”
J. Biomech.
35
,
347
353
(
2002
).
76.
N. D.
Broom
, “
The stress/strain and fatigue behaviour of glutaraldehyde preserved heart-valve tissue
,”
J. Biomech.
10
,
707
724
(
1977
).
77.
N. D.
Broom
, “
Fatigue-induced damage in glutaraldehyde-preserved heart valve tissue
,”
J. Thorac. Cardiovasc. Surg.
76
,
202
211
(
1978
).
78.
J. M.
Paez
,
A. C.
Sanmartín
,
E. J.
Herrero
,
I.
Millan
,
A.
Cordon
,
A.
Rocha
,
M.
Maestro
,
R.
Burgos
,
G.
Tellez
, and
J. L.
Castillo-Olivares
, “
Durability of a cardiac valve leaflet made of calf pericardium: Fatigue and energy consumption
,”
J. Biomed. Mater. Res. A
77
,
839
849
(
2006
).
79.
T. L.
Sellaro
,
D.
Hildebrand
,
Q.
Lu
,
N.
Vyavahare
,
M.
Scott
, and
M. S.
Sacks
, “
Effects of collagen fiber orientation on the response of biologically derived soft tissue biomaterials to cyclic loading
,”
J. Biomed. Mater. Res. A
80
,
194
205
(
2007
).
80.
C.
Martin
and
W.
Sun
, “
Modeling of long-term fatigue damage of soft tissue with stress softening and permanent set effects
,”
Biomech. Model. Mechanobiol.
12
,
645
655
(
2013
).
81.
C. C.
Church
, “
A theoretical study of cavitation generated by an extracorporeal shock wave lithotripter
,”
J. Acoust. Soc. Am.
86
(
1
),
215
227
(
1989
).
82.
R. O.
Cleveland
,
M. R.
Bailey
,
N.
Fineberg
,
B.
Hartenbaum
,
M.
Lokhandwalla
,
J. A.
McAteer
, and
B.
Sturtevant
, “
Design and characterization of a research electrohydraulic lithotripter patterned after the Dornier HM3
,”
Rev. Sci. Instrum.
71
,
2514
2525
(
2000
).
83.
M.
Lokhandwalla
,
J. A.
McAteer
,
J. C.
Williams
, Jr.
, and
B.
Sturtevant
, “
Mechanical haemolysis in shock wave lithotripsy (SWL): II. In vitro cell lysis due to shear
,”
Phys. Med. Biol.
46
,
1245
1264
(
2001
).
84.
J. B.
Freund
,
T.
Colonius
, and
A. P.
Evan
, “
A cumulative shear mechanism for tissue damage initiation in shock-wave lithotripsy
,”
Ultrasound Med. Biol.
33
,
1495
1503
(
2007
).
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