Abstract

Laser-generated focused ultrasound (LGFU) is a unique modality that can produce single-pulsed cavitation and strong local disturbances on a tight focal spot (<100 μm). We utilize LGFU as a non-contact, non-thermal, high-precision tool to fractionate and cleave cell clusters cultured on glass substrates. Fractionation processes are investigated in detail, which confirms distinct cell behaviors in the focal center and the periphery of LGFU spot. For better understanding of local disturbances under LGFU, we use a high-speed laser-flash shadowgraphy technique and then fully visualize instantaneous microscopic processes from the ultrasound wave focusing to the micro-bubble collapse. Based on these visual evidences, we discuss possible mechanisms responsible for the focal and peripheral disruptions, such as a liquid jet-induced wall shear stress and shock emissions due to bubble collapse. The ultrasonic micro-fractionation is readily available for in vitro cell patterning and harvesting. Moreover, it is significant as a preliminary step towards high-precision surgery applications in future.

© 2013 OSA

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2012 (2)

A. Maxwell, O. Sapozhnikov, M. Bailey, L. Crum, Z. Xu, B. Fowlkes, C. Cain, and V. Khokhlova, “Disintegration of tissue using high intensity focused ultrasound: two approaches that utilize shock waves,” Acou. Today8(4), 24–37 (2012).
[CrossRef]

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

2011 (3)

J. J. Rassweiler, T. Knoll, K.-U. Köhrmann, J. A. McAteer, J. E. Lingeman, R. O. Cleveland, M. R. Bailey, and C. Chaussy, “Shock wave technology and application: an update,” Eur. Urol.59(5), 784–796 (2011).
[CrossRef] [PubMed]

Y.-F. Zhou, “High intensity focused ultrasound in clinical tumor ablation,” World J Clin Oncol2(1), 8–27 (2011).
[CrossRef] [PubMed]

D. G. Shchukin, E. Skorb, V. Belova, and H. Möhwald, “Ultrasonic cavitation at solid surfaces,” Adv. Mater.23(17), 1922–1934 (2011).
[CrossRef] [PubMed]

2010 (2)

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett.97(23), 234104 (2010).
[CrossRef] [PubMed]

T. Lee, D. Jang, D. Ahn, and D. Kim, “Effect of liquid environment on laser-induced backside wet etching of fused silica,” J. Appl. Phys.107(3), 033112 (2010).
[CrossRef]

2009 (2)

J. E. Lingeman, J. A. McAteer, E. Gnessin, and A. P. Evan, “Shock wave lithotripsy: advances in technology and technique,” Nat Rev Urol6(12), 660–670 (2009).
[CrossRef] [PubMed]

C. Goldenstedt, A. Birer, D. Cathignol, and C. Lafon, “Blood clot disruption in vitro using shockwaves delivered by an extracorporeal generator after pre-exposure to lytic agent,” Ultrasound Med. Biol.35(6), 985–990 (2009).
[CrossRef] [PubMed]

2008 (3)

T. J. Dubinsky, C. Cuevas, M. K. Dighe, O. Kolokythas, and J. H. Hwang, “High-intensity focused ultrasound: current potential and oncologic applications,” AJR Am. J. Roentgenol.190(1), 191–199 (2008).
[CrossRef] [PubMed]

C. C. Coussios and R. A. Roy, “Applications of acoustics and cavitation to noninvasive therapy and drug delivery,” Annu. Rev. Fluid Mech.40(1), 395–420 (2008).
[CrossRef]

R. Dijkink, S. Le Gac, E. Nijhuis, A. van den Berg, I. Vermes, A. Poot, and C.-D. Ohl, “Controlled cavitation-cell interaction: trans-membrane transport and viability studies,” Phys. Med. Biol.53(2), 375–390 (2008).
[CrossRef] [PubMed]

2007 (2)

E. Zwaan, S. Le Gac, K. Tsuji, and C.-D. Ohl, “Controlled cavitation in microfluidic systems,” Phys. Rev. Lett.98(25), 254501 (2007).
[CrossRef] [PubMed]

G. T. Haar and C. Coussios, “High intensity focused ultrasound: physical principles and devices,” Int. J. Hyperthermia23(2), 89–104 (2007).
[CrossRef] [PubMed]

2006 (3)

K. R. Rau, P. A. Quinto-Su, A. N. Hellman, and V. Venugopalan, “Pulsed laser microbeam-induced cell lysis: time-resolved imaging and analysis of hydrodynamic effects,” Biophys. J.91(1), 317–329 (2006).
[CrossRef] [PubMed]

E. Herbert, S. Balibar, and F. Caupin, “Cavitation pressure in water,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.74(4), 041603 (2006).
[CrossRef] [PubMed]

C.-D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse, “Sonoporation from jetting cavitation bubbles,” Biophys. J.91(11), 4285–4295 (2006).
[CrossRef] [PubMed]

2005 (2)

Z. Xu, J. B. Fowlkes, E. D. Rothman, A. M. Levin, and C. A. Cain, “Controlled ultrasound tissue erosion: The role of dynamic interaction between insonation and microbubble activity,” J. Acoust. Soc. Am.117(1), 424–435 (2005).
[CrossRef] [PubMed]

J. E. Kennedy, “High-intensity focused ultrasound in the treatment of solid tumours,” Nat. Rev. Cancer5(4), 321–327 (2005).
[CrossRef] [PubMed]

2004 (1)

Z. Xu, A. Ludomirsky, L. Y. Eun, T. L. Hall, B. C. Tran, J. B. Fowlkes, and C. A. Cain, “Controlled ultrasound tissue erosion,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(6), 726–736 (2004).
[CrossRef] [PubMed]

2003 (2)

C.-D. Ohl and B. Wolfrum, “Detachment and sonoporation of adherent HeLa-cells by shock wave-induced cavitation,” Biochim. Biophys. Acta1624(1-3), 131–138 (2003).
[CrossRef] [PubMed]

L. Junge, C. D. Ohl, B. Wolfrum, M. Arora, and R. Ikink, “Cell detachment method using shock-wave-induced cavitation,” Ultrasound Med. Biol.29(12), 1769–1776 (2003).
[CrossRef] [PubMed]

2000 (1)

T. D. Mast, “Empirical relationships between acoustic parameters in human soft tissues,” ARLO1(2), 37 (2000).
[CrossRef]

Ahn, D.

T. Lee, D. Jang, D. Ahn, and D. Kim, “Effect of liquid environment on laser-induced backside wet etching of fused silica,” J. Appl. Phys.107(3), 033112 (2010).
[CrossRef]

Arora, M.

C.-D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse, “Sonoporation from jetting cavitation bubbles,” Biophys. J.91(11), 4285–4295 (2006).
[CrossRef] [PubMed]

L. Junge, C. D. Ohl, B. Wolfrum, M. Arora, and R. Ikink, “Cell detachment method using shock-wave-induced cavitation,” Ultrasound Med. Biol.29(12), 1769–1776 (2003).
[CrossRef] [PubMed]

Baac, H. W.

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

Bailey, M.

A. Maxwell, O. Sapozhnikov, M. Bailey, L. Crum, Z. Xu, B. Fowlkes, C. Cain, and V. Khokhlova, “Disintegration of tissue using high intensity focused ultrasound: two approaches that utilize shock waves,” Acou. Today8(4), 24–37 (2012).
[CrossRef]

Bailey, M. R.

J. J. Rassweiler, T. Knoll, K.-U. Köhrmann, J. A. McAteer, J. E. Lingeman, R. O. Cleveland, M. R. Bailey, and C. Chaussy, “Shock wave technology and application: an update,” Eur. Urol.59(5), 784–796 (2011).
[CrossRef] [PubMed]

Balibar, S.

E. Herbert, S. Balibar, and F. Caupin, “Cavitation pressure in water,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.74(4), 041603 (2006).
[CrossRef] [PubMed]

Belova, V.

D. G. Shchukin, E. Skorb, V. Belova, and H. Möhwald, “Ultrasonic cavitation at solid surfaces,” Adv. Mater.23(17), 1922–1934 (2011).
[CrossRef] [PubMed]

Birer, A.

C. Goldenstedt, A. Birer, D. Cathignol, and C. Lafon, “Blood clot disruption in vitro using shockwaves delivered by an extracorporeal generator after pre-exposure to lytic agent,” Ultrasound Med. Biol.35(6), 985–990 (2009).
[CrossRef] [PubMed]

Cain, C.

A. Maxwell, O. Sapozhnikov, M. Bailey, L. Crum, Z. Xu, B. Fowlkes, C. Cain, and V. Khokhlova, “Disintegration of tissue using high intensity focused ultrasound: two approaches that utilize shock waves,” Acou. Today8(4), 24–37 (2012).
[CrossRef]

Cain, C. A.

Z. Xu, J. B. Fowlkes, E. D. Rothman, A. M. Levin, and C. A. Cain, “Controlled ultrasound tissue erosion: The role of dynamic interaction between insonation and microbubble activity,” J. Acoust. Soc. Am.117(1), 424–435 (2005).
[CrossRef] [PubMed]

Z. Xu, A. Ludomirsky, L. Y. Eun, T. L. Hall, B. C. Tran, J. B. Fowlkes, and C. A. Cain, “Controlled ultrasound tissue erosion,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(6), 726–736 (2004).
[CrossRef] [PubMed]

Cathignol, D.

C. Goldenstedt, A. Birer, D. Cathignol, and C. Lafon, “Blood clot disruption in vitro using shockwaves delivered by an extracorporeal generator after pre-exposure to lytic agent,” Ultrasound Med. Biol.35(6), 985–990 (2009).
[CrossRef] [PubMed]

Caupin, F.

E. Herbert, S. Balibar, and F. Caupin, “Cavitation pressure in water,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.74(4), 041603 (2006).
[CrossRef] [PubMed]

Chaussy, C.

J. J. Rassweiler, T. Knoll, K.-U. Köhrmann, J. A. McAteer, J. E. Lingeman, R. O. Cleveland, M. R. Bailey, and C. Chaussy, “Shock wave technology and application: an update,” Eur. Urol.59(5), 784–796 (2011).
[CrossRef] [PubMed]

Chen, S.-L.

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett.97(23), 234104 (2010).
[CrossRef] [PubMed]

Chen, Y.-C.

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

Cleveland, R. O.

J. J. Rassweiler, T. Knoll, K.-U. Köhrmann, J. A. McAteer, J. E. Lingeman, R. O. Cleveland, M. R. Bailey, and C. Chaussy, “Shock wave technology and application: an update,” Eur. Urol.59(5), 784–796 (2011).
[CrossRef] [PubMed]

Coussios, C.

G. T. Haar and C. Coussios, “High intensity focused ultrasound: physical principles and devices,” Int. J. Hyperthermia23(2), 89–104 (2007).
[CrossRef] [PubMed]

Coussios, C. C.

C. C. Coussios and R. A. Roy, “Applications of acoustics and cavitation to noninvasive therapy and drug delivery,” Annu. Rev. Fluid Mech.40(1), 395–420 (2008).
[CrossRef]

Crum, L.

A. Maxwell, O. Sapozhnikov, M. Bailey, L. Crum, Z. Xu, B. Fowlkes, C. Cain, and V. Khokhlova, “Disintegration of tissue using high intensity focused ultrasound: two approaches that utilize shock waves,” Acou. Today8(4), 24–37 (2012).
[CrossRef]

Cuevas, C.

T. J. Dubinsky, C. Cuevas, M. K. Dighe, O. Kolokythas, and J. H. Hwang, “High-intensity focused ultrasound: current potential and oncologic applications,” AJR Am. J. Roentgenol.190(1), 191–199 (2008).
[CrossRef] [PubMed]

de Jong, N.

C.-D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse, “Sonoporation from jetting cavitation bubbles,” Biophys. J.91(11), 4285–4295 (2006).
[CrossRef] [PubMed]

Delius, M.

C.-D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse, “Sonoporation from jetting cavitation bubbles,” Biophys. J.91(11), 4285–4295 (2006).
[CrossRef] [PubMed]

Dighe, M. K.

T. J. Dubinsky, C. Cuevas, M. K. Dighe, O. Kolokythas, and J. H. Hwang, “High-intensity focused ultrasound: current potential and oncologic applications,” AJR Am. J. Roentgenol.190(1), 191–199 (2008).
[CrossRef] [PubMed]

Dijkink, R.

R. Dijkink, S. Le Gac, E. Nijhuis, A. van den Berg, I. Vermes, A. Poot, and C.-D. Ohl, “Controlled cavitation-cell interaction: trans-membrane transport and viability studies,” Phys. Med. Biol.53(2), 375–390 (2008).
[CrossRef] [PubMed]

Dubinsky, T. J.

T. J. Dubinsky, C. Cuevas, M. K. Dighe, O. Kolokythas, and J. H. Hwang, “High-intensity focused ultrasound: current potential and oncologic applications,” AJR Am. J. Roentgenol.190(1), 191–199 (2008).
[CrossRef] [PubMed]

Eun, L. Y.

Z. Xu, A. Ludomirsky, L. Y. Eun, T. L. Hall, B. C. Tran, J. B. Fowlkes, and C. A. Cain, “Controlled ultrasound tissue erosion,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(6), 726–736 (2004).
[CrossRef] [PubMed]

Evan, A. P.

J. E. Lingeman, J. A. McAteer, E. Gnessin, and A. P. Evan, “Shock wave lithotripsy: advances in technology and technique,” Nat Rev Urol6(12), 660–670 (2009).
[CrossRef] [PubMed]

Fowlkes, B.

A. Maxwell, O. Sapozhnikov, M. Bailey, L. Crum, Z. Xu, B. Fowlkes, C. Cain, and V. Khokhlova, “Disintegration of tissue using high intensity focused ultrasound: two approaches that utilize shock waves,” Acou. Today8(4), 24–37 (2012).
[CrossRef]

Fowlkes, J. B.

Z. Xu, J. B. Fowlkes, E. D. Rothman, A. M. Levin, and C. A. Cain, “Controlled ultrasound tissue erosion: The role of dynamic interaction between insonation and microbubble activity,” J. Acoust. Soc. Am.117(1), 424–435 (2005).
[CrossRef] [PubMed]

Z. Xu, A. Ludomirsky, L. Y. Eun, T. L. Hall, B. C. Tran, J. B. Fowlkes, and C. A. Cain, “Controlled ultrasound tissue erosion,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(6), 726–736 (2004).
[CrossRef] [PubMed]

Gnessin, E.

J. E. Lingeman, J. A. McAteer, E. Gnessin, and A. P. Evan, “Shock wave lithotripsy: advances in technology and technique,” Nat Rev Urol6(12), 660–670 (2009).
[CrossRef] [PubMed]

Goldenstedt, C.

C. Goldenstedt, A. Birer, D. Cathignol, and C. Lafon, “Blood clot disruption in vitro using shockwaves delivered by an extracorporeal generator after pre-exposure to lytic agent,” Ultrasound Med. Biol.35(6), 985–990 (2009).
[CrossRef] [PubMed]

Guo, L. J.

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett.97(23), 234104 (2010).
[CrossRef] [PubMed]

Haar, G. T.

G. T. Haar and C. Coussios, “High intensity focused ultrasound: physical principles and devices,” Int. J. Hyperthermia23(2), 89–104 (2007).
[CrossRef] [PubMed]

Hall, T. L.

Z. Xu, A. Ludomirsky, L. Y. Eun, T. L. Hall, B. C. Tran, J. B. Fowlkes, and C. A. Cain, “Controlled ultrasound tissue erosion,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(6), 726–736 (2004).
[CrossRef] [PubMed]

Hart, A. J.

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett.97(23), 234104 (2010).
[CrossRef] [PubMed]

Hellman, A. N.

K. R. Rau, P. A. Quinto-Su, A. N. Hellman, and V. Venugopalan, “Pulsed laser microbeam-induced cell lysis: time-resolved imaging and analysis of hydrodynamic effects,” Biophys. J.91(1), 317–329 (2006).
[CrossRef] [PubMed]

Herbert, E.

E. Herbert, S. Balibar, and F. Caupin, “Cavitation pressure in water,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.74(4), 041603 (2006).
[CrossRef] [PubMed]

Hwang, J. H.

T. J. Dubinsky, C. Cuevas, M. K. Dighe, O. Kolokythas, and J. H. Hwang, “High-intensity focused ultrasound: current potential and oncologic applications,” AJR Am. J. Roentgenol.190(1), 191–199 (2008).
[CrossRef] [PubMed]

Ikink, R.

C.-D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse, “Sonoporation from jetting cavitation bubbles,” Biophys. J.91(11), 4285–4295 (2006).
[CrossRef] [PubMed]

L. Junge, C. D. Ohl, B. Wolfrum, M. Arora, and R. Ikink, “Cell detachment method using shock-wave-induced cavitation,” Ultrasound Med. Biol.29(12), 1769–1776 (2003).
[CrossRef] [PubMed]

Jang, D.

T. Lee, D. Jang, D. Ahn, and D. Kim, “Effect of liquid environment on laser-induced backside wet etching of fused silica,” J. Appl. Phys.107(3), 033112 (2010).
[CrossRef]

Junge, L.

L. Junge, C. D. Ohl, B. Wolfrum, M. Arora, and R. Ikink, “Cell detachment method using shock-wave-induced cavitation,” Ultrasound Med. Biol.29(12), 1769–1776 (2003).
[CrossRef] [PubMed]

Kennedy, J. E.

J. E. Kennedy, “High-intensity focused ultrasound in the treatment of solid tumours,” Nat. Rev. Cancer5(4), 321–327 (2005).
[CrossRef] [PubMed]

Khokhlova, V.

A. Maxwell, O. Sapozhnikov, M. Bailey, L. Crum, Z. Xu, B. Fowlkes, C. Cain, and V. Khokhlova, “Disintegration of tissue using high intensity focused ultrasound: two approaches that utilize shock waves,” Acou. Today8(4), 24–37 (2012).
[CrossRef]

Kim, D.

T. Lee, D. Jang, D. Ahn, and D. Kim, “Effect of liquid environment on laser-induced backside wet etching of fused silica,” J. Appl. Phys.107(3), 033112 (2010).
[CrossRef]

Knoll, T.

J. J. Rassweiler, T. Knoll, K.-U. Köhrmann, J. A. McAteer, J. E. Lingeman, R. O. Cleveland, M. R. Bailey, and C. Chaussy, “Shock wave technology and application: an update,” Eur. Urol.59(5), 784–796 (2011).
[CrossRef] [PubMed]

Köhrmann, K.-U.

J. J. Rassweiler, T. Knoll, K.-U. Köhrmann, J. A. McAteer, J. E. Lingeman, R. O. Cleveland, M. R. Bailey, and C. Chaussy, “Shock wave technology and application: an update,” Eur. Urol.59(5), 784–796 (2011).
[CrossRef] [PubMed]

Kolokythas, O.

T. J. Dubinsky, C. Cuevas, M. K. Dighe, O. Kolokythas, and J. H. Hwang, “High-intensity focused ultrasound: current potential and oncologic applications,” AJR Am. J. Roentgenol.190(1), 191–199 (2008).
[CrossRef] [PubMed]

Lafon, C.

C. Goldenstedt, A. Birer, D. Cathignol, and C. Lafon, “Blood clot disruption in vitro using shockwaves delivered by an extracorporeal generator after pre-exposure to lytic agent,” Ultrasound Med. Biol.35(6), 985–990 (2009).
[CrossRef] [PubMed]

Le Gac, S.

R. Dijkink, S. Le Gac, E. Nijhuis, A. van den Berg, I. Vermes, A. Poot, and C.-D. Ohl, “Controlled cavitation-cell interaction: trans-membrane transport and viability studies,” Phys. Med. Biol.53(2), 375–390 (2008).
[CrossRef] [PubMed]

E. Zwaan, S. Le Gac, K. Tsuji, and C.-D. Ohl, “Controlled cavitation in microfluidic systems,” Phys. Rev. Lett.98(25), 254501 (2007).
[CrossRef] [PubMed]

Lee, K.-T.

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

Lee, T.

T. Lee, D. Jang, D. Ahn, and D. Kim, “Effect of liquid environment on laser-induced backside wet etching of fused silica,” J. Appl. Phys.107(3), 033112 (2010).
[CrossRef]

Levin, A. M.

Z. Xu, J. B. Fowlkes, E. D. Rothman, A. M. Levin, and C. A. Cain, “Controlled ultrasound tissue erosion: The role of dynamic interaction between insonation and microbubble activity,” J. Acoust. Soc. Am.117(1), 424–435 (2005).
[CrossRef] [PubMed]

Ling, T.

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett.97(23), 234104 (2010).
[CrossRef] [PubMed]

Lingeman, J. E.

J. J. Rassweiler, T. Knoll, K.-U. Köhrmann, J. A. McAteer, J. E. Lingeman, R. O. Cleveland, M. R. Bailey, and C. Chaussy, “Shock wave technology and application: an update,” Eur. Urol.59(5), 784–796 (2011).
[CrossRef] [PubMed]

J. E. Lingeman, J. A. McAteer, E. Gnessin, and A. P. Evan, “Shock wave lithotripsy: advances in technology and technique,” Nat Rev Urol6(12), 660–670 (2009).
[CrossRef] [PubMed]

Lohse, D.

C.-D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse, “Sonoporation from jetting cavitation bubbles,” Biophys. J.91(11), 4285–4295 (2006).
[CrossRef] [PubMed]

Ludomirsky, A.

Z. Xu, A. Ludomirsky, L. Y. Eun, T. L. Hall, B. C. Tran, J. B. Fowlkes, and C. A. Cain, “Controlled ultrasound tissue erosion,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(6), 726–736 (2004).
[CrossRef] [PubMed]

Mast, T. D.

T. D. Mast, “Empirical relationships between acoustic parameters in human soft tissues,” ARLO1(2), 37 (2000).
[CrossRef]

Maxwell, A.

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

A. Maxwell, O. Sapozhnikov, M. Bailey, L. Crum, Z. Xu, B. Fowlkes, C. Cain, and V. Khokhlova, “Disintegration of tissue using high intensity focused ultrasound: two approaches that utilize shock waves,” Acou. Today8(4), 24–37 (2012).
[CrossRef]

McAteer, J. A.

J. J. Rassweiler, T. Knoll, K.-U. Köhrmann, J. A. McAteer, J. E. Lingeman, R. O. Cleveland, M. R. Bailey, and C. Chaussy, “Shock wave technology and application: an update,” Eur. Urol.59(5), 784–796 (2011).
[CrossRef] [PubMed]

J. E. Lingeman, J. A. McAteer, E. Gnessin, and A. P. Evan, “Shock wave lithotripsy: advances in technology and technique,” Nat Rev Urol6(12), 660–670 (2009).
[CrossRef] [PubMed]

Möhwald, H.

D. G. Shchukin, E. Skorb, V. Belova, and H. Möhwald, “Ultrasonic cavitation at solid surfaces,” Adv. Mater.23(17), 1922–1934 (2011).
[CrossRef] [PubMed]

Nijhuis, E.

R. Dijkink, S. Le Gac, E. Nijhuis, A. van den Berg, I. Vermes, A. Poot, and C.-D. Ohl, “Controlled cavitation-cell interaction: trans-membrane transport and viability studies,” Phys. Med. Biol.53(2), 375–390 (2008).
[CrossRef] [PubMed]

Ohl, C. D.

L. Junge, C. D. Ohl, B. Wolfrum, M. Arora, and R. Ikink, “Cell detachment method using shock-wave-induced cavitation,” Ultrasound Med. Biol.29(12), 1769–1776 (2003).
[CrossRef] [PubMed]

Ohl, C.-D.

R. Dijkink, S. Le Gac, E. Nijhuis, A. van den Berg, I. Vermes, A. Poot, and C.-D. Ohl, “Controlled cavitation-cell interaction: trans-membrane transport and viability studies,” Phys. Med. Biol.53(2), 375–390 (2008).
[CrossRef] [PubMed]

E. Zwaan, S. Le Gac, K. Tsuji, and C.-D. Ohl, “Controlled cavitation in microfluidic systems,” Phys. Rev. Lett.98(25), 254501 (2007).
[CrossRef] [PubMed]

C.-D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse, “Sonoporation from jetting cavitation bubbles,” Biophys. J.91(11), 4285–4295 (2006).
[CrossRef] [PubMed]

C.-D. Ohl and B. Wolfrum, “Detachment and sonoporation of adherent HeLa-cells by shock wave-induced cavitation,” Biochim. Biophys. Acta1624(1-3), 131–138 (2003).
[CrossRef] [PubMed]

Ok, J. G.

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett.97(23), 234104 (2010).
[CrossRef] [PubMed]

Park, H. J.

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett.97(23), 234104 (2010).
[CrossRef] [PubMed]

Poot, A.

R. Dijkink, S. Le Gac, E. Nijhuis, A. van den Berg, I. Vermes, A. Poot, and C.-D. Ohl, “Controlled cavitation-cell interaction: trans-membrane transport and viability studies,” Phys. Med. Biol.53(2), 375–390 (2008).
[CrossRef] [PubMed]

Quinto-Su, P. A.

K. R. Rau, P. A. Quinto-Su, A. N. Hellman, and V. Venugopalan, “Pulsed laser microbeam-induced cell lysis: time-resolved imaging and analysis of hydrodynamic effects,” Biophys. J.91(1), 317–329 (2006).
[CrossRef] [PubMed]

Rassweiler, J. J.

J. J. Rassweiler, T. Knoll, K.-U. Köhrmann, J. A. McAteer, J. E. Lingeman, R. O. Cleveland, M. R. Bailey, and C. Chaussy, “Shock wave technology and application: an update,” Eur. Urol.59(5), 784–796 (2011).
[CrossRef] [PubMed]

Rau, K. R.

K. R. Rau, P. A. Quinto-Su, A. N. Hellman, and V. Venugopalan, “Pulsed laser microbeam-induced cell lysis: time-resolved imaging and analysis of hydrodynamic effects,” Biophys. J.91(1), 317–329 (2006).
[CrossRef] [PubMed]

Rothman, E. D.

Z. Xu, J. B. Fowlkes, E. D. Rothman, A. M. Levin, and C. A. Cain, “Controlled ultrasound tissue erosion: The role of dynamic interaction between insonation and microbubble activity,” J. Acoust. Soc. Am.117(1), 424–435 (2005).
[CrossRef] [PubMed]

Roy, R. A.

C. C. Coussios and R. A. Roy, “Applications of acoustics and cavitation to noninvasive therapy and drug delivery,” Annu. Rev. Fluid Mech.40(1), 395–420 (2008).
[CrossRef]

Sapozhnikov, O.

A. Maxwell, O. Sapozhnikov, M. Bailey, L. Crum, Z. Xu, B. Fowlkes, C. Cain, and V. Khokhlova, “Disintegration of tissue using high intensity focused ultrasound: two approaches that utilize shock waves,” Acou. Today8(4), 24–37 (2012).
[CrossRef]

Shchukin, D. G.

D. G. Shchukin, E. Skorb, V. Belova, and H. Möhwald, “Ultrasonic cavitation at solid surfaces,” Adv. Mater.23(17), 1922–1934 (2011).
[CrossRef] [PubMed]

Skorb, E.

D. G. Shchukin, E. Skorb, V. Belova, and H. Möhwald, “Ultrasonic cavitation at solid surfaces,” Adv. Mater.23(17), 1922–1934 (2011).
[CrossRef] [PubMed]

Tran, B. C.

Z. Xu, A. Ludomirsky, L. Y. Eun, T. L. Hall, B. C. Tran, J. B. Fowlkes, and C. A. Cain, “Controlled ultrasound tissue erosion,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(6), 726–736 (2004).
[CrossRef] [PubMed]

Tsuji, K.

E. Zwaan, S. Le Gac, K. Tsuji, and C.-D. Ohl, “Controlled cavitation in microfluidic systems,” Phys. Rev. Lett.98(25), 254501 (2007).
[CrossRef] [PubMed]

van den Berg, A.

R. Dijkink, S. Le Gac, E. Nijhuis, A. van den Berg, I. Vermes, A. Poot, and C.-D. Ohl, “Controlled cavitation-cell interaction: trans-membrane transport and viability studies,” Phys. Med. Biol.53(2), 375–390 (2008).
[CrossRef] [PubMed]

Venugopalan, V.

K. R. Rau, P. A. Quinto-Su, A. N. Hellman, and V. Venugopalan, “Pulsed laser microbeam-induced cell lysis: time-resolved imaging and analysis of hydrodynamic effects,” Biophys. J.91(1), 317–329 (2006).
[CrossRef] [PubMed]

Vermes, I.

R. Dijkink, S. Le Gac, E. Nijhuis, A. van den Berg, I. Vermes, A. Poot, and C.-D. Ohl, “Controlled cavitation-cell interaction: trans-membrane transport and viability studies,” Phys. Med. Biol.53(2), 375–390 (2008).
[CrossRef] [PubMed]

Versluis, M.

C.-D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse, “Sonoporation from jetting cavitation bubbles,” Biophys. J.91(11), 4285–4295 (2006).
[CrossRef] [PubMed]

Wolfrum, B.

L. Junge, C. D. Ohl, B. Wolfrum, M. Arora, and R. Ikink, “Cell detachment method using shock-wave-induced cavitation,” Ultrasound Med. Biol.29(12), 1769–1776 (2003).
[CrossRef] [PubMed]

C.-D. Ohl and B. Wolfrum, “Detachment and sonoporation of adherent HeLa-cells by shock wave-induced cavitation,” Biochim. Biophys. Acta1624(1-3), 131–138 (2003).
[CrossRef] [PubMed]

Won Baac, H.

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett.97(23), 234104 (2010).
[CrossRef] [PubMed]

Xu, Z.

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

A. Maxwell, O. Sapozhnikov, M. Bailey, L. Crum, Z. Xu, B. Fowlkes, C. Cain, and V. Khokhlova, “Disintegration of tissue using high intensity focused ultrasound: two approaches that utilize shock waves,” Acou. Today8(4), 24–37 (2012).
[CrossRef]

Z. Xu, J. B. Fowlkes, E. D. Rothman, A. M. Levin, and C. A. Cain, “Controlled ultrasound tissue erosion: The role of dynamic interaction between insonation and microbubble activity,” J. Acoust. Soc. Am.117(1), 424–435 (2005).
[CrossRef] [PubMed]

Z. Xu, A. Ludomirsky, L. Y. Eun, T. L. Hall, B. C. Tran, J. B. Fowlkes, and C. A. Cain, “Controlled ultrasound tissue erosion,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(6), 726–736 (2004).
[CrossRef] [PubMed]

Yoon, E.

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

Zhou, Y.-F.

Y.-F. Zhou, “High intensity focused ultrasound in clinical tumor ablation,” World J Clin Oncol2(1), 8–27 (2011).
[CrossRef] [PubMed]

Zwaan, E.

E. Zwaan, S. Le Gac, K. Tsuji, and C.-D. Ohl, “Controlled cavitation in microfluidic systems,” Phys. Rev. Lett.98(25), 254501 (2007).
[CrossRef] [PubMed]

Acou. Today (1)

A. Maxwell, O. Sapozhnikov, M. Bailey, L. Crum, Z. Xu, B. Fowlkes, C. Cain, and V. Khokhlova, “Disintegration of tissue using high intensity focused ultrasound: two approaches that utilize shock waves,” Acou. Today8(4), 24–37 (2012).
[CrossRef]

Adv. Mater. (1)

D. G. Shchukin, E. Skorb, V. Belova, and H. Möhwald, “Ultrasonic cavitation at solid surfaces,” Adv. Mater.23(17), 1922–1934 (2011).
[CrossRef] [PubMed]

AJR Am. J. Roentgenol. (1)

T. J. Dubinsky, C. Cuevas, M. K. Dighe, O. Kolokythas, and J. H. Hwang, “High-intensity focused ultrasound: current potential and oncologic applications,” AJR Am. J. Roentgenol.190(1), 191–199 (2008).
[CrossRef] [PubMed]

Annu. Rev. Fluid Mech. (1)

C. C. Coussios and R. A. Roy, “Applications of acoustics and cavitation to noninvasive therapy and drug delivery,” Annu. Rev. Fluid Mech.40(1), 395–420 (2008).
[CrossRef]

Appl. Phys. Lett. (1)

H. Won Baac, J. G. Ok, H. J. Park, T. Ling, S.-L. Chen, A. J. Hart, and L. J. Guo, “Carbon nanotube composite optoacoustic transmitters for strong and high frequency ultrasound generation,” Appl. Phys. Lett.97(23), 234104 (2010).
[CrossRef] [PubMed]

ARLO (1)

T. D. Mast, “Empirical relationships between acoustic parameters in human soft tissues,” ARLO1(2), 37 (2000).
[CrossRef]

Biochim. Biophys. Acta (1)

C.-D. Ohl and B. Wolfrum, “Detachment and sonoporation of adherent HeLa-cells by shock wave-induced cavitation,” Biochim. Biophys. Acta1624(1-3), 131–138 (2003).
[CrossRef] [PubMed]

Biophys. J. (2)

C.-D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, and D. Lohse, “Sonoporation from jetting cavitation bubbles,” Biophys. J.91(11), 4285–4295 (2006).
[CrossRef] [PubMed]

K. R. Rau, P. A. Quinto-Su, A. N. Hellman, and V. Venugopalan, “Pulsed laser microbeam-induced cell lysis: time-resolved imaging and analysis of hydrodynamic effects,” Biophys. J.91(1), 317–329 (2006).
[CrossRef] [PubMed]

Eur. Urol. (1)

J. J. Rassweiler, T. Knoll, K.-U. Köhrmann, J. A. McAteer, J. E. Lingeman, R. O. Cleveland, M. R. Bailey, and C. Chaussy, “Shock wave technology and application: an update,” Eur. Urol.59(5), 784–796 (2011).
[CrossRef] [PubMed]

IEEE Trans. Ultrason. Ferroelectr. Freq. Control (1)

Z. Xu, A. Ludomirsky, L. Y. Eun, T. L. Hall, B. C. Tran, J. B. Fowlkes, and C. A. Cain, “Controlled ultrasound tissue erosion,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(6), 726–736 (2004).
[CrossRef] [PubMed]

Int. J. Hyperthermia (1)

G. T. Haar and C. Coussios, “High intensity focused ultrasound: physical principles and devices,” Int. J. Hyperthermia23(2), 89–104 (2007).
[CrossRef] [PubMed]

J. Acoust. Soc. Am. (1)

Z. Xu, J. B. Fowlkes, E. D. Rothman, A. M. Levin, and C. A. Cain, “Controlled ultrasound tissue erosion: The role of dynamic interaction between insonation and microbubble activity,” J. Acoust. Soc. Am.117(1), 424–435 (2005).
[CrossRef] [PubMed]

J. Appl. Phys. (1)

T. Lee, D. Jang, D. Ahn, and D. Kim, “Effect of liquid environment on laser-induced backside wet etching of fused silica,” J. Appl. Phys.107(3), 033112 (2010).
[CrossRef]

Nat Rev Urol (1)

J. E. Lingeman, J. A. McAteer, E. Gnessin, and A. P. Evan, “Shock wave lithotripsy: advances in technology and technique,” Nat Rev Urol6(12), 660–670 (2009).
[CrossRef] [PubMed]

Nat. Rev. Cancer (1)

J. E. Kennedy, “High-intensity focused ultrasound in the treatment of solid tumours,” Nat. Rev. Cancer5(4), 321–327 (2005).
[CrossRef] [PubMed]

Phys. Med. Biol. (1)

R. Dijkink, S. Le Gac, E. Nijhuis, A. van den Berg, I. Vermes, A. Poot, and C.-D. Ohl, “Controlled cavitation-cell interaction: trans-membrane transport and viability studies,” Phys. Med. Biol.53(2), 375–390 (2008).
[CrossRef] [PubMed]

Phys. Rev. E Stat. Nonlin. Soft Matter Phys. (1)

E. Herbert, S. Balibar, and F. Caupin, “Cavitation pressure in water,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys.74(4), 041603 (2006).
[CrossRef] [PubMed]

Phys. Rev. Lett. (1)

E. Zwaan, S. Le Gac, K. Tsuji, and C.-D. Ohl, “Controlled cavitation in microfluidic systems,” Phys. Rev. Lett.98(25), 254501 (2007).
[CrossRef] [PubMed]

Sci Rep (1)

H. W. Baac, J. G. Ok, A. Maxwell, K.-T. Lee, Y.-C. Chen, A. J. Hart, Z. Xu, E. Yoon, and L. J. Guo, “Carbon-nanotube optoacoustic lens for focused ultrasound generation and high-precision targeted therapy,” Sci Rep2, 989 (2012).
[CrossRef] [PubMed]

Ultrasound Med. Biol. (2)

L. Junge, C. D. Ohl, B. Wolfrum, M. Arora, and R. Ikink, “Cell detachment method using shock-wave-induced cavitation,” Ultrasound Med. Biol.29(12), 1769–1776 (2003).
[CrossRef] [PubMed]

C. Goldenstedt, A. Birer, D. Cathignol, and C. Lafon, “Blood clot disruption in vitro using shockwaves delivered by an extracorporeal generator after pre-exposure to lytic agent,” Ultrasound Med. Biol.35(6), 985–990 (2009).
[CrossRef] [PubMed]

World J Clin Oncol (1)

Y.-F. Zhou, “High intensity focused ultrasound in clinical tumor ablation,” World J Clin Oncol2(1), 8–27 (2011).
[CrossRef] [PubMed]

Other (2)

A. D. Maxwell, “Noninvasive thrombolysis using histotripsy pulsed ultrasound cavitation therapy,” Ph.D. Thesis, University of Michigan (2012).

H. W. Baac, J. Frampton, J. G. Ok, S. Takayama, and L. J. Guo, “Localized micro-scale disruption of cells using laser-generated focused ultrasound,” J. Biophoton. doi: (2013).
[CrossRef]

Supplementary Material (1)

» Media 1: MOV (4323 KB)     

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Figures (4)

Fig. 1
Fig. 1

Experimental schematics. (a) A setup for micro-fractionation of cell clusters by LGFU. The setup was prepared on the inverted microscope (BE: beam expander, F: optical filter, HL: halogen lamp, L: objective lens, M: mirror, ND: neutral density filter, OL: optoacoustic lens, PL: Nd:YAG pulsed laser beam (6-ns pulse width), S: supporting frame,). (b) A shadowgraphic imaging setup (LD: laser diode, OSC: digital oscilloscope, PD: photodetector, Probe: probe laser beam (1-ns pulse width), SP: supporting plate, TRG/DL: trigger and delay-generator unit, ZL: zoom lens).

Fig. 2
Fig. 2

Demonstration of micro-fractionation by LGFU (Media 1) (scale bar = 100 μm). The LGFU spot is fixed while the cell culture plate is slowly moved to the upper-right direction (a-e). For convenience, the disruption zones are guided by the inner and outer circles (35 and 90 μm in diameter, respectively). A captured time (t) is shown on the right-top corner (unit: second): (a) The cultured cell cluster is shown with a target spot; (b) Under LGFU, the cluster is fractionated primarily at the focal center; (c) The prolonged exposure of LGFU enlarges the fractionated zone over the periphery; (c-e) As we move the cluster, LGFU finally cleaves it into two pieces.

Fig. 3
Fig. 3

Micro-fractionation process in a sparse cell network that is used for distinctive morphology deformation (scale bar = 100 μm; inner and outer circle diameters = 35 and 90 μm; time t (second)): (a) The LGFU spot was positioned at the cell-cell junction; (b) In a short time, the junction is sharply cut by LGFU at the focal center; (c) The spot is re-positioned slightly to the rightward direction; (c)-(e) The spot stays at the same position to observe the peripheral disruption effects under prolonged LGFU. The cells are pushed away along the radial directions (arrows in (d)), and their retreatment is clearly shown in (e) (compare with (c)), indicated by two small arrows. Also, the cell-cell connection is pulled away along the bi-directional arrow.

Fig. 4
Fig. 4

Shadowgraphic imaging of LGFU-induced disruptions (all scale bars: 100 μm). Instantaneous images are shown sequentially. A captured time is shown on the left bottom (unit: μs) as relatively defined from the moment of cavitation inception. The fiber thickness is 125 μm for all figures: (a1-a3) Incidence of LGFU from the left to the right. The wavefronts are indicated by the arrows; (b1-b3) Tiny bubbles generated under LGFU with the outgoing pressure wave (thin red arrow); (c1-c2) A cloud formation by the merged bubbles; (c3-c4) Shrinkage steps; (d1) A collapse-induced shock is shown as the spherical wavefront (arrow); (d2) Shock propagation is shown by the left arrow (a direct outgoing wave) and the right arrow (a reflected wave from the substrate).

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