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Abstract
Lately, a fiber-based optical tweezer that traps and arranges the micro/nano-particles is crucial in practical applications, because such a device can trap the biological samples and drive them to the designated position in a microfluidic system or vessel without harming them. Here, we report a new type of fiber optical tweezer, which can trap and arrange erythrocytes. It is prepared by coating graphene on the cross section of a microfiber. Our results demonstrate that thermal-gradient-induced natural convection flow and thermophoresis can trap the erythrocytes under low incident power, and the optical scattering force can arrange them precisely under higher incident power. The proposed optical tweezer has high flexibility, easy fabrication, and high integration with lab-on-a-chip, and shows considerable potential for application in various fields, such as biophysics, biochemistry, and life sciences.
© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement
1. Introduction
Optical tweezers have served as effective and convenient tools for trapping and manipulation of microscale dielectric particles [1–3], especially by natural convection flow [4] or optical forces [5–7] induced by laser light irradiation. This approach has been developed for several decades and is widely applied in physics [4], biochemistry [8], and life sciences [9]. Especially in medical and biological research, cell-cell contacts have been proven crucial for determining the suppression of neoplastic phenotype [10], activating microRNA biogenesis [11], preparing spheroids composed of primary cancer cells [12], etc. However, most biological cells have weak light-matter interactions because of their low refractive index contrast [13], resulting in weak trapping strengths. Increasing the incident irradiation to acquire stronger trapping strength can harm the cells. Therefore, the efficient trapping and arrangement of cells without harming them remains a challenge [14]. Recently, researchers demonstrated that the efficient use of thermal effects induced by optical absorption could effectively improve the optical trapping capability [15–22]. As the temperature increases in the illuminated zone, the combined effect of thermophoresis and natural convection flow drags the particles into the hotter region. Interestingly, graphene, a monolayer of hexagonally arranged carbon atoms [23], has high thermal and electric conductivity [24], which indicates that it is a good candidate for efficient trapping of cells based on the photothermal effect.
Lately, fiber-based optical tweezers have drawn increasing attention owing to their compact, versatile, and portable structure and their ability to be remotely controlled [25]. In addition, fiber optical tweezer systems are readily integrated into lab-on-a-chip devices, which can reduce the required intensity of incident light as well as eliminate the necessity for bulky optics [26,27]. Especially, it has been shown that fiber optical tweezers are a feasible way to trap particles by the photothermal effect [28,29] or drive micro-objects by the optical scattering force [30,31]. Heretofore, fiber optical tweezers were used for either trapping or driving the particles. The combined functionalities of trapping and driving in a single device has rarely been reported, although it is immensely useful in a microfluidic system because it can trap biological samples and drive them to a designated position without harming them. In addition, particle arrangement with high precision, especially in the case of particles of the size of several microns, is important for biological applications and biophotonic integrations [32]. As native optical materials, cells are widely used for manipulating light by means of cell chains. Previous studies have experimentally demonstrated that the living cell arrangements, such as, red blood cells, yeast cells, and Escherichia coli cells, can be integrated into functionalized devices to realize optical trapping [33,34] as well as various applications, such as, force probes [9], biophotonic waveguides [35], and optofluidic microlenses [36]. Therefore, a tapered fiber optical tweezer that can trap and arrange biological particles is strongly desired.
Here, we present an easily fabricated fiber-based optical tweezer by coating graphene on a microfiber probe. The graphene-coated microfiber probe (GCMP) can effectively trap erythrocytes by thermophoresis and natural convection flow (Fig. 1(a)) and arrange them over a long distance by the optical scattering force (Fig. 1(b)) without injury. We employ finite element simulations to study the underlying mechanisms, such as, natural convection flow, thermophoresis, and optical scattering force. The optical strategy presented in this work is expected to lay a solid foundation for further applications of other sub-micron particles and biological samples in a mixture or human blood solution by changing the parameters of the GCMP.
Fig. 1 Experimental configuration of the trapping and arrangement of erythrocytes by GCMP. (a) Schematic illustration of the natural convection flow and thermophoresis; (b) Schematic illustration of the arrangement along with the propagating beam; (c) Optical microscope image of GCMP; (d) SEM image of the graphene coated on the cross section of the microfiber; (e) Schematic of the experimental setup. A 980-nm laser light is focused on the GCMP, which is immersed in an erythrocyte suspension. The fiber tip is sheathed by a glass capillary and is easily manipulated by a six-axis manipulator. A microscope with a CCD camera is used for observation, image capture, and real-time recording. (f) AFM image of an erythrocyte.
2. Experimental details
We prepared a fiber taper by using a commercial single-mode optical fiber (connector type: FC/PC, core diameter: 9 μm, cladding diameter: 125 μm; Corning Inc.) based on the flame-heating technique [19]. For the preparation of the GCMP, a graphene nanosheet suspension in ethanol solution (0.5 mg/mL) is filled in a pipette and poured dropwise on the end face of a microfiber probe, which is fixed vertically with a fiber positioner. Meanwhile, a 1550-nm laser beam with an incident power of 20 mW is focused on the fiber. The graphene nanosheets are thus irradiated by the light and tightly adsorbed on the cross section of the microfiber with the volatilization of ethanol and form a uniform micro-sized graphene film because of the high imaginary part of the refractive index of graphene () [37]. The thickness of the graphene nanosheets can be well controlled by varying the concentrations of graphene in the ethanol solution. Figure 1(c) presents the optical image of the GCMP and Fig. 1(d) shows the scanning electron microscopy (SEM) image of graphene on the cross section of the microfiber. The image reveals good morphological stability. The diameter of the GCMP gradually decreases from 10.45 μm to 9.55 μm within a length of 52 μm, and then an abruptly tapering section appears. As shown in Fig. 1(d), a homogeneous thin graphene layer is deposited on the cross section of the microfiber and serves as a microlens. Because of the relatively high thermal conductivity of graphene [37], the light absorption results in significant heat generation, inducing a temperature gradient and a natural convection flow. Meanwhile, the large real part of the refractive index of graphene causes a tightly focused beam to be generated along the light propagation path because of the constructive interference of the optical field. Figure 1(e) shows the schematic of the experimental setup. A 980-nm laser, which is weakly absorbed by biological matter, is coupled with the prepared single-mode fiber as a GCMP. The end of the GCMP is immersed in an aqueous suspension of erythrocytes on a SiO2 substrate. The atomic force microscope (AFM) image in Fig. 1(f) reveals the morphology of a 6.0-μm-diameter erythrocyte with a doughnut-type structure, obtained from an adult mouse.
Figures 2(a)-2(e) exhibit the trapping process of erythrocytes with incident power of P = 8 mW to experimentally investigate the temperature gradient, natural convection flow, and the capture of erythrocytes. When the GCMP is excited by a 980-nm laser, a large temperature gradient appears around the fiber taper owing to the photothermal effects of graphene; then, a strong natural convection flow causes the erythrocytes to move across a large distance toward the hot center (> 95 μm) while the thermophoretic force, which acts in the opposite direction to the convection flow, prevents the erythrocytes from being pushed beyond the hot center [17,38]. Finally, the trapped particles automatically form a tightly packed assembly. The experiment was recorded with a CCD video camera (Visualization 1) with a 10 × objective lens. The video presents a stable three-dimensional trapping of the erythrocytes by the GCMP. Figure 2(f) shows a rapid linear trapping ability of the GCMP with a slope of 0.657, presented as a function of the time for which light is incident on the GCMP. An average arrival velocity of ~18.34 μm/s is observed in the trapping experiment by monitoring the particle movements through frame-by-frame analysis of the video images in Visualization 1. Briefly, the trapping process demonstrates that the high optical absorption of graphene results in significant natural convection flow and thermophoresis. This induces stable trapping of the particles under low incident power, which is larger than that possible with plasmonic nanostructures [14,22].
Fig. 2 Sequence of optical microscope images recorded for erythrocyte trapping based on natural convection flow and thermophoresis. (a)-(e) Sequential steps of the trapping process under incident power of 8 mW, which are recorded in detail in Visualization 1. The white arrows denote the direction of particle trapping. (f) Number of assembled erythrocytes as a function of time under incident power of 8 mW.
With further increase in the incident power to 12 mW, the trapped erythrocytes around the tip of the GCMP are pushed away along the path of light propagation and a cell chain is formed by arrangement, as shown in Figs. 3(a)-3(d). The chain length grows to 52.17 μm within 70.1 s, and further increases to 56.23 μm after 50.9 s at an average velocity of 0.08 μm/s, as shown in Fig. 3(i). Meanwhile, the number of erythrocytes aggregating around the tip (indicated by the red circle) increases noticeably at P = 12 mW. As the number of trapped erythrocytes increases, the erythrocytes close to the tip are squeezed and gradually move along in the direction of light propagation, which extends the chain of erythrocytes and forms a bio-waveguide (see details in Visualization 2). Further increase in the power from 12 to 20 mW results in the aggregation and accelerated pushing of the erythrocytes, as shown in Figs. 3(e)-3(h). The erythrocyte chain increases from 58.26 μm at t = 147.0 s to 68.70 μm at t = 188.5 s with an average velocity of 0.24 μm/s, as shown in Fig. 3(i). When the incident power increases from 12 to 20 mW, the pushing ability is enhanced by approximately three times, whereas the trapping ability is suppressed from 0.136 to 0.103, as shown in Fig. 3(j). This phenomenon can be well explained by the saturation of the light absorption capability of graphene. With the increase in the incident power, the light absorbed by graphene reaches the saturation absorption threshold; then, the excess light is focused on the shadow-side surface of graphene from where it generates a propagating beam. Meanwhile, the gradient optical force along the direction of light propagation is larger than the natural convection flow and the thermophoretic force in the opposite direction, resulting in the erythrocytes being pushed along the light propagation direction, as illustrated in Fig. 1(b). This endows the ability of the GCMP to trap the erythrocytes under low incident power and the ability to arrange them under high incident power.
Fig. 3 Sequences of optical microscope images recorded for erythrocyte arrangement based on pushing ability. (a)-(d) Erythrocyte trapping and arrangement processes at different instances of time as the incident power increases to 12 mW, which is recorded in detail in Visualization 2. (e)-(h) The corresponding process with increase in incident power to 20 mW. The trapped erythrocytes are indicated by red circles. The navy blue arrows denote the direction in which the erythrocytes are pushed. (i) Average velocity of erythrocytes under the pushing effect along the light propagation direction under optical power of 12 and 20 mW. (j) Number of assembled erythrocytes as a function of time under the incident power of 12 and 20 mW.
3. Discussion
To further explain the above phenomena, three-dimensional (3D) finite element simulation (COMSOL Multiphysics 5.1) was used to simulate the distributions of the optical energy, thermal field, and optical forces [39]. At a free-space wavelength of 980 nm, the refractive indexes of water, graphene, erythrocyte, and fiber are 1.33, 2.60, 1.573, and 1.445, respectively. Based on stationary Maxwell’s equations, the temperature of the electromagnetic heat source from graphene can be calculated by
where Qe represents the heat energy from graphene, J is the free charge density, E*/H* is the complex conjugate intensity of the electric/magnetic field, ω is the angular frequency of the electromagnetic wave, B is the intensity of magnetic induction, k is the thermal conductivity, T is the temperature, is the temperature gradient, and Cp is the heat capacity. It is well known that the excellent thermal conductivity (~600 Wm−1 K−1) of graphene [37] is helpful in generating uniform heating and natural convection flow for trapping of particles. Meanwhile, the interaction between the evanescent fields of the GCMP and the dielectric micro-object produces different optical forces. To numerically show the pushing ability, the optical force exerted on a single particle can be expressed aswhere n is the surface normal vector. The integration is performed over a closed surface S surrounding the particle. The integral of the Maxwell stress tensor can be written aswhere I is a unit dyadic, and ε and μ are the electric permittivity and magnetic permeability of the surrounding, respectively. Based on this result, the calculated Fx (Fy) is the component of F in the x(y)-direction. In this simulation, the excitation is a transverse-electric (TE) polarization at a wavelength of 980 nm. Based on the obtained non-zero electromagnetic field components Ez, Hx, and Hy, the components Fx and Fy can be expressed as [31]To quantitatively understand the effect of the natural convection flow and thermophoretic force on the particles, the local temperature and velocity distributions of the convection are calculated and shown in Fig. 4. In the model, the GCMP is immersed in an aqueous solution. The ambient temperature distribution of GCMP with the initial environmental temperature as 293 K (room temperature) is shown in Fig. 4(a). As the GCMP is excited by a 980-nm laser of 10-mW power, there is a small range of localized temperature increment induced by the focusing of the laser beam around the fiber tip (Fig. 4(a) and Table 1). The ambient temperature decreases rapidly from 296.2 K to 293 K over a distance d of ~50 μm away from the fiber tip, as shown in the inset of Fig. 4(a). Meanwhile, as the incident power increases stepwise from 0 to 20 mW, the temperature of the graphene surface increases from room temperature to approximately 296.2 K at P = 10 mW, and remains constant when the incident power is increased further (Fig. 4(b)). The temperature saturation point induces the largest natural convection flow and thermophoresis occurs at the incident power of 10 mW, which agrees with the experimental results in Figs. 3(a)-3(d). Because of the thinness of the graphene film and high specific heat capacity of water, the heat produced can be transferred rapidly, which further confirms that such a small temperature increment has no obvious harmful effects on the biological cells during the experiment. The above results are also in good agreement with the experimental results reported in [40].
Fig. 4 Theoretical simulation of GCMP. (a) Calculated temperature distribution induced by the focusing of the 980-nm laser beam on the coated graphene at incident power of 10 mW. The inset shows ambient temperature as a function of distance d to graphene along x axis. (b) Temperature variation as a function of laser power of the hot zone; (c, d) Top (c) and cross section (d) views of fluidic velocity distributions on the free surface.
Table 1. Comparison of optical functions, temperature increment (ΔT), maximum optical force (Fmax), and required minimum incident power (Pmax) with those of similar optical tweezer devices reported in literature.
Next, the top and cross section views of the velocity distribution of the vortex were simulated under the incident power of 10 mW, as shown in Figs. 4(c) and 4(d). Here, based on the temperature gradient, the vortex can maintain stability in the three-dimensional space and control the particles at the vortex center. Furthermore, the vertical drag force F in the vortex center region can be obtained using Stokes law F = μv, where μ = 3πεηD is a coefficient, η is the dynamic viscosity, D is the diameter of the erythrocytes, v is the velocity of the erythrocyte, and ε = 2.67 [41] is a correction factor accounting for the particle proximity to the substrate. The final estimated convective drag force obtained using η = ∼0.98 × 10−3 Ns/m2 at temperature of 296 K is ~2.7 pN, which is smaller than that of plasmonic random nanostructures (Table 1). Furthermore, the calculated dimensionless quantity Q = ~−0.19, obtained from the expression Q = cF/nP [42], reveals the high-efficiency trapping performed by this device. The observations also demonstrate the close dependence of temperature on the incident power.
Besides the natural convection flow and thermophoresis, we theoretically studied the optical scattering force on the erythrocytes, which is responsible for arranging them. The calculated electric field amplitude (EA) distribution and optical forces exerted on the particles along the x- and y-axis were simulated at the incident power of 10 mW. Figure 5(a) shows EA with full-width at half-maximum of 4.16 μm and working distance length (WDL) of approximately 56 μm when the thickness and diameter of graphene are 0.5 μm and 9 μm, respectively. The intensity of light focused at the near field is 1.4 times that of the incident light, indicating larger scattering force. Figures 5(b) and 5(c) represent the EA distributions for particles located at the focus and side focus sites. As shown in Fig. 5(b), the erythrocyte can increase the difference between the intensities of the two sides because of the bio-microlens effect [37]. The light intensity in this case is stronger on the right side (shaded side) than on the left side (illuminated side) along the x-axis, inducing larger optical scattering force Fx directed along the light propagation direction. Similar, Fy is perpendicular to the x-axis because of the asymmetrical light intensities on the two sides (Fig. 5(c)). In order to obtain a clear picture, the intensity of EA and the scattering force Fx as functions of the distance along the x-axis are calculated and presented in Fig. 5(d). The positive Fx value indicates that the force is delivered along the light propagation direction and has a value larger than 100 pN/W at the near field and decreases rapidly at x > 40 μm owing to the smaller EA. Notably, the combined action of the convection flow and thermophoretic force restricts the movement of the particles to a slow velocity. The symmetrical distributions of EA and Fy at x = 16.75 μm are presented in Fig. 5(e). EA exhibits a Gaussian distribution and leads to a central symmetrical distribution of the trapping force (Fy) at y = 0. In the distribution region, the large Fy is directed along the x-axis with a dominating gradient force Fg. Far away from the x-axis, Fy is too small to trap the particles because of the weak light intensity. Therefore, the optical scattering force can provide a stable pushing force and form a bio-waveguide through the self-assembly of erythrocytes, as shown in Fig. 3.
Fig. 5 (a) Calculated EA; (b, c) EA for particle located at (16.75 μm, 0) (b) and (16.75 μm, 3 μm) (c); (d) Force Fx exerted on particles in (b) along the x-axis; (e) transverse optical force (Fy).
4. Conclusions
We systematically investigated the erythrocyte manipulation by a fiber optical tweezer prepared by graphene coated on the cross section of a microfiber. The natural convection flow and thermophoresis induced by local heating from the absorption of light by graphene results in the trapping of the erythrocytes under low incident power. Under larger incident power, the saturation of light absorption by graphene causes the optical scattering force to become larger than the convection flow and thermophoretic force, thus pushing the cells along the light propagation direction and arranging the cells as a bio-waveguide. In the manipulation of the trapping and arrangement process, a small temperature increment of ~3 °C causes no harm to the biological cells. Our results indicate that the families of carbon-based materials, such as, graphene oxide and carbon nanotube, which possess high thermal and electric conductivity, can be expected to exhibit similar properties as graphene and manifest the benefits of thermophoresis and optical scattering force in fiber-based optical tweezer. Our proposed GCMP has the advantages of high flexibility, easy fabrication, and high integration with lab-on-a-chip, and exhibits great potential for application in biophysics, biochemistry, life sciences, and biophotonics.
Funding
National Natural Science Foundation of China (NSFC) (11874157, 61574065, 51603069, 11621101, 81630046, 61627827, 91539127); Guangdong Natural Science Foundation (2017B030301007, 2016A020221030, 2016B090906004, 2016TQ03R749); National Key Research and Development Program of China (2017YFA0205700); Natural Science Foundation of Guizhou Province ([2016]1150 and [2015]67); Science and technology project of Guangzhou (Grant No. 201805010002); Talent Project of Guangdong Industry Polytechnic (KYRC2017-0018).
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