Neutrophil-inspired propulsion in a combined acoustic and magnetic field

Abstract

Systems capable of precise motion in the vasculature can offer exciting possibilities for applications in targeted therapeutics and non-invasive surgery. So far, the majority of the work analysed propulsion in a two-dimensional setting with limited controllability near boundaries. Here we show bio-inspired rolling motion by introducing superparamagnetic particles in magnetic and acoustic fields, inspired by a neutrophil rolling on a wall. The particles self-assemble due to dipole-dipole interaction in the presence of a rotating magnetic field. The aggregate migrates towards the wall of the channel due to the radiation force of an acoustic field. By combining both fields, we achieved a rolling-type motion along the boundaries. The use of both acoustic and magnetic fields has matured in clinical settings. The combination of both fields is capable of overcoming the limitations encountered by single actuation techniques. We believe our method will have far-reaching implications in targeted therapeutics.Devising effective swimming and propulsion strategies in microenvironments is attractive for drug delivery applications. Here Ahmed et al. demonstrate a micropropulsion strategy in which a combination of magnetic and acoustic fields is used to assemble and propel colloidal particles along channel walls.

Fig. 1

Neutrophil-inspired propulsion based on acoustic and magnetic field actuation. a Neutrophil rolls on vasculature before transmigrating into tissue. b Superparamagnetic particles aggregate due to dipole–dipole interaction in the presence of a magnetic field (i). The aggregate migrates towards the wall due to the radiation force in an acoustic field (ii). A rolling-type motion along the boundary is achieved by combining both fields. The assembled entities disassociate when the magnetic field is turned off

Fig. 2

Analysis of particle trapping. a A schematic demonstrates the radiation force (F _R) and the sidewall-induced streaming drag (F _AS) that act on different sized particles. Large particles, which are illustrated in red, migrate to the channel sidewall by the radiation force. Small particles, which are shown in green, follow sidewall-induced streaming. b For a particle with a diameter a < a _c, the acoustic streaming force dominates. c For a particle with a diameter a > a _c, the acoustic radiation force dominates. d The plot shows the ratio of the acoustic radiation to streaming forces vs. different size polystyrene particle for various geometry factor, Ψ. Above the black line, F _R > F _AS, i.e. radiation force dominates and below the line, F _R < F _AS, i.e. streaming dominates. e The plot demonstrates the competing forces of the polystyrene (PS) and the superparamagnetic particles (SP) at Ψ ~0.4

Fig. 3

Particle–wall interaction in an acoustic field. Image sequences demonstrate the particle–wall interaction of a 1, b 3, c 6, d 10 and e 15.5 μm diameter polystyrene particles, respectively, in a microfluidic channel. a–c Represents the sidewall-induced acoustic streaming developed within the microchannel. The vortex width w decreases with increasing particle diameter. d, e Demonstrates migration and trapping of 10 and 15.5 μm particles, respectively, at the channel sidewalls (see also Supplementary Movie 1). Blue arrows represent the particle trajectories, t ₀ and t ₁ represent the initial and final position, respectively. Scale bar, 50 µm

Fig. 4

Particle interaction in a rotating magnetic field. a 1–2 µm fluorescent superparamagnetic particles are dispersed within the glass slides in the absence of a magnetic field. b The superparamagnetic particles self-assemble and form spinning chains at a rotational frequency of 0.1 Hz. c The spinning chains fragment into satellites, and eventually the chain transforms into spinning orbits at a higher frequency. The rotation of the spinning aggregates is demonstrated at a rotational frequency of 20 Hz, see also Supplementary Movie 3. Scale bar, 100 µm

Fig. 5

Rolling motion in acoustic and magnetic fields. a The 1–2 µm superparamagnetic particles self-assemble and form spinning aggregates rotating in the clockwise direction in the presence of a magnetic field. b The aggregate migrates towards the channel wall due to the radiation force of an acoustic field. c Image sequence demonstrates the rolling-type propulsion along the sidewall of the microfluidic channel (Supplementary Movie 4). d The superparamagnetic particles disassociate as soon as the magnetic field is turned off. Scale bar of b–d is 50 µm. e Image sequence demonstrates the counter-clockwise motion of an aggregate and executing rolling when reached the wall under a magnetic field strength and rotation frequency of 20 mT and 20 Hz, respectively, at an acoustic driving voltage of 20 V_PP (Supplementary Movie 6). Scale bar, 25 µm. f The plot of the rolling velocity against acoustic driving voltage at magnetic rotational frequencies (m _f) of 7.5, 15 and 22 Hz, respectively, at 15 mT, of 2.9 µm superparamagnetic particles. Each data point represents the average rolling velocity analysed from 3–5 swimmers except data points at 10 V_PP. The error bar represents the standard deviation (s.d.). g An aggregate is shown weak to no rolling at low-acoustic driving voltages of 10 V_PP under a magnetic field strength and rotation frequency of 15 mT and 7.5 Hz, respectively (Supplementary Movie 7). Scale bar, 25 µm

Fig. 6

Propulsion in a circular cross-sectional artificial vasculature. a The image represents a three-dimensional PDMS-based artificial vasculature with a circular cross section. The inset shows the fluorescently labelled channel. b The particles sediment vertically downward towards the nearest surface and then slowly roll down to the bottom of the channel due to gravity. c Particles roll up along the circular channel from state t ₀ to t ₁ in the presence of acoustic waves. The green dashed line in c represents the maximum height particles can reach. d Particle rolls down along the surface, from state t ₀ to t ₁ in the absence of acoustic waves. e The micrograph shows that particles aligned at the bottom of the channel in the absence of the acoustic waves. f Image sequence demonstrates the particles migration is moving upwards along the channel in the presence of the acoustic field, see also Supplementary Movie 8. g Rolling motion is executed in a circular channel, see also Supplementary Movie 9. All scale bars, 500 µm