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

Miller, Morton W.; Miller, Douglas L.; Brayman, Andrew A.

doi:10.1016/s0301-5629(96)00089-0

Cited by 468 publications

(259 citation statements)

References 124 publications

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“…Cell damage due to radial motion of the extracellular flow-field has already been suggested earlier (Carstensen et al 1993, Miller et al 1996, but a detailed interaction of this extracellular flow-field with a cell is presented here for the first time. The objective of this work is to analyse deformation of a cell subjected to a general flow-field.…”

Section: Introductionmentioning

confidence: 92%

Mechanical haemolysis in shock wave lithotripsy (SWL): I. Analysis of cell deformation due to SWL flow-fields

Lokhandwalla¹,

Sturtevant²

2001

Phys. Med. Biol.

105

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This work analyses the interaction of red blood cells (RBCs) with shock-induced and bubble-induced flows in shock wave lithotripsy (SWL), and calculates, in vitro, the lytic effects of these two flows. A well known experimentally observed fact about RBC membranes is that the lipid bilayer disrupts when subjected to an areal strain ( A/A) c of 3%, and a corresponding, critical, isotropic tension, T c , of 10 mN m −1 (1 mN m −1 = 1 dyne cm −1 ). RBCs suspended in a fluid medium tend to deform in accordance with the deformation of the surrounding fluid medium. The fluid flow-field is lytically effective if the membrane deformation exceeds the above threshold value.From kinematic analysis, motion of an elementary fluid particle can always be decomposed into a uniform translation, an extensional flow (e.g. u ∞ (x, y, z) = (k(t)x, −k(t)y, 0)) along three mutually perpendicular axes, and a rigid rotation of these axes. However, only an extensional flow causes deformation of a fluid particle, and consequently deforms the RBC membrane. In SWL, a fluid flow-field, induced by a non-uniform shock wave, as well as radial expansion/implosion of a bubble, has been hypothesized to cause lysis of cells. Both the above flow-fields constitute an unsteady, extensional flow, which exerts inertial as well as viscous forces on the RBC membrane. The transient inertial force (expressed as a tension, or force/length), is given by T iner ∼ ρr 3 c k/τ , where τ is a timescale of the transient flow and r c is a characteristic cell size. When the membrane is deformed due to inertial effects, membrane strain is given by A/A ∼ kτ . The transient viscous force is given by T visc ∼ ρ(ν/τ ) 1/2 r 2 c k, where ρ and ν are the fluid density and kinematic viscosity. For the non-uniform shock, the extensional flow exerts an inertial force, T iner ≈ 64 mN m −1 , for a duration of 3 ns, sufficient to induce pores in the RBC membrane. For a radial flow-field, induced by bubble expansion/implosion, the inertial forces are of a magnitude 100 mN m −1 , which last for a duration of 1 µs, sufficient to cause rupture. Bubble-induced radial flow is predicted to be

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Section: Introductionmentioning

confidence: 92%

Mechanical haemolysis in shock wave lithotripsy (SWL): I. Analysis of cell deformation due to SWL flow-fields

Lokhandwalla¹,

Sturtevant²

2001

Phys. Med. Biol.

105

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“…It has been found that sonoporation is enhanced significantly when cavitation bubbles are present during the acoustic exposure, suggesting that a fluid dynamic interaction between cavitation bubbles and cells is responsible for membrane poration [17,31,32], The physical mechanism of sonoporation is not well understood and thus the dependence of membrane permeabilization on the cavitation parameters is not yet known [33,34], A better understanding of the physical mechanisms responsible for the poration of the cell membrane is crucial for the optimization of this technique. As a result many groups are examining ultrasound-generated cavitation bubble dynamics and the resulting fluid velocities to determine the shear stresses and exposure times required to achieve sonoporation, cell detachment, and cell lysis [16,17,29,35,36].…”

Section: Implications For Molecular Delivery and Acoustic Cavitation mentioning

confidence: 99%

Biophysical Response to Pulsed Laser Microbeam‐Induced Cell Lysis and Molecular Delivery

Hellman

Rau

Yoon

et al. 2008

Journal of Biophotonics

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Cell lysis and molecular delivery in confluent monolayers of PtK 2 cells are achieved by the delivery of 6 ns, λ = 532 nm laser pulses via a 40×, 0.8 NA microscope objective. With increasing distance from the point of laser focus we find regions of (a) immediate cell lysis; (b) necrotic cells that detach during the fluorescence assays; (c) permeabilized cells sufficient to facilitate the uptake of small (3kDa) FITC-conjugated Dextran molecules in viable cells; and (d) unaffected, viable cells. The spatial extent of cell lysis, cell detachment, and molecular delivery increased with laser pulse energy. Hydrodynamic analysis from time-resolved imaging studies reveal that the maximum wall shear stress associated with the pulsed laser microbeam-induced cavitation bubble expansion governs the location and spatial extent of each of these regions independent of laser pulse energy. Specifically, cells exposed to maximum wall shear stresses τ w, max > 190 ± 20 kPa are immediately lysed while cells exposed to τ w, max > 18 ± 2kPa are necrotic and subsequently detach. Cells exposed to τ w, max in the range 8-18 kPa are viable and successfully optoporated with 3kDa Dextran molecules. Cells exposed to τ w, max < 8 ± 1 kPa remain viable without molecular delivery. These findings provide the first direct correlation between pulsed laser microbeam-induced shear stresses and subsequent cellular outcome.

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“…26,[29][30][31][32] Cavitation involves the formation of gaseous bubbles, a few micrometers in diameter, because of a disruption of the propagation medium by the negative pressure cycle in ultrasonic fields. 38 These cavitation bubbles can oscillate in response to ultrasound fields, possibly influencing the surrounding structures such as membranes. Alternatively, they can have effects on the tissue including tumor Figure 6 Histology of rat carotids (H&E, top 2 Â , bottom 20 Â ).…”

Section: Discussionmentioning

confidence: 99%

Focused ultrasound (HIFU) induces localized enhancement of reporter gene expression in rabbit carotid artery

et al. 2003

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The development of accurate, safe, and efficient gene delivery remains a major challenge towards the realization of gene therapeutic prevention and treatment of cardiovascular diseases. In this study, we investigated the ability of high-intensity focused ultrasound (HIFU), a form of mechanical wave transmission, to act as a noninvasive tool for the enhancement of in vivo gene transfer into rabbit carotid arteries. Segments of the common carotid arteries of New Zealand white rabbits were isolated and infused with plasmid DNA encoding the reporter b-galactosidase either with or without the addition of ultrasound contrast agent consisting of small (B2-5 mm) gasfilled human albumin microspheres to augment cavitation. Infused arteries were exposed to pulsed ultrasound for 1 min (frequency 0.85 MHz, burst length 50 ms, repetition frequency 1 Hz, duration 60 s, peak pressure amplitude of 15 MPa). At 6.3 MPa, HIFU enhanced gene expression eight-fold, and 17.5-fold in the presence of contrast. We found increasing amounts of b-galactosidase expression in the carotid vessel with increasing pressure amplitude. This dose-response relation was present with and without contrast. Without contrast, no vessel damage was detected up to 15 MPa, while the addition of contrast induced side effects above a threshold of 6.3 MPa peak pressure. The entire procedure was feasible and safe for the animals, and the results suggest that HIFU has the potential to assist in the noninvasive spatial regulation of gene transfer into the vascular system.

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

Cited by 468 publications

References 124 publications

Mechanical haemolysis in shock wave lithotripsy (SWL): I. Analysis of cell deformation due to SWL flow-fields

Mechanical haemolysis in shock wave lithotripsy (SWL): I. Analysis of cell deformation due to SWL flow-fields

Biophysical Response to Pulsed Laser Microbeam‐Induced Cell Lysis and Molecular Delivery

Focused ultrasound (HIFU) induces localized enhancement of reporter gene expression in rabbit carotid artery

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