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© 2013 The Authors. Published by WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 5863
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Sangwon Kim , Famin Qiu , Samhwan Kim , Ali Ghanbari , Cheil Moon , Li Zhang ,
Bradley J. Nelson , * and Hongsoo Choi *
Fabrication and Characterization of Magnetic Microrobots
for Three-Dimensional Cell Culture and
Targeted Transportation
S. Kim, Dr. A. Ghanbari, Prof. B. J. Nelson, Prof. H. Choi
Robotics Engineering Department
Daegu Gyeongbuk Institute of Science and
Technology (DGIST),
711-873, Daegu, South Korea
E-mail: bnelson@ethz.ch; mems@dgist.ac.kr
F. Qiu, Prof. B. J. Nelson
Institute of Robotics and Intelligent Systems
ETH Zurich, Zurich
CH-8092, Switzerland
S. Kim, Prof. C. Moon
Brain Science Department
Daegu Gyeongbuk Institute of Science and Technology (DGIST)
711-873, Daegu, South Korea
Prof. L. Zhang
Department of Mechanical and Automation Engineering
The Chinese University of Hong Kong
Hong Kong SAR, China
This is an open access article under the terms of the Creative Commons
Attribution-NonCommercial-NoDerivs Licence, which permits use and
distribution in any medium, provided the original work is properly cited,
the use is non-commercial and no modifi cations or adaptations are made.
DOI: 10.1002/adma.201301484
Medical microrobots are being widely studied for specifi c appli-
cations, such as targeted drug delivery, biopsy, hyperthermia,
radioactive therapy, scaffolding, in-vivo ablation, stenting,
sensing, and marking.
[ 1 ] These operations can be carried out
with microrobots that offer a minimally invasive, accurately
targeted, localized therapy via wireless intervention, such as
magnetic fi elds.
[ 2–5 ] Numerous studies have examined the bio-
medical applications of magnetic actuation. Magnetic tubes
and rotors have been developed for sensitive engines and fl uid
mixers driven by magnetic actuation.
[ 6–9 ] Among the various
applications proposed for medical micro-devices, targeted drug
delivery and micro-object transportation can be implemented
using biocompatible and magnetically actuated agents. In pre-
vious studies, nanoparticles, magnetic particles, and nickel
nanowires have been used as platforms for drug delivery.
[ 10–13 ]
Helical and tubular lipid microstructures were developed as
drug delivery platforms to overcome problems such as the poor
loading capacity and propulsion effi ciency.
[ 14 ] For helical micro-
robots,
[ 15–20 ] rotational motion induces translational velocity,
which is one of the most effective propulsion methods in the
low Reynolds number regime.
[ 21–24 ] To transport cells using
magnetically actuated helical swimmers, a magnetized polymer
helix, equipped with a cell gripper, is controlled by external
magnetic fi elds.
[ 20 ] These helical microrobots have been used to
transport a single microsphere in three dimensions. The micro-
robots were coated with a thin titanium (Ti) layer for better
biocompatibility and affi nity with the cells; this was confi rmed
by culturing cells on the helical microrobots. Similarly, micro-
spheres can be transported in the fl owing streams of micro-
fl uidic channels, which enable the microrobots to swim in the
dynamic fl ow in the microfl uidic channel.
[ 25 ]
This paper reports the fabrication and characterization of
three-dimensional (3D) porous micro-niches as a transporter
using a photocurable polymer. The structures were coated with
nickel (Ni) for magnetic actuation, and with Ti to ensure bio-
compatibility for possible in-vivo applications. The fabricated
microrobots were rotated wirelessly and translated using a
magnetic manipulator. Translational velocities were measured
experimentally for different magnetic fi eld gradients in the hor-
izontal direction when the microrobots were aligned in vertical
direction. Complex manipulations were also demonstrated by
synchronized swimming and targeted tracking. Human embry-
onic kidney (HEK) 293 cells were cultured with the microrobot
to demonstrate the feasibility of using microrobots as multi-
cell transporters. Compared with previous microrobotic cargo
devices, a well-defi ned 3D porous structure was used to culture
multiple cells inside a structure with a customized pore size. A
microrobot containing cells inside can be controlled magneti-
cally in body fl uids such as blood, urine, cerebrospinal fl uid,
or vitreous humor, to transport the cells to a target position in
the body.
A scaffold is a porous 3D structure that is used for cell
adhesion and mechanical support for tissue and organ regen-
eration.
[ 26–29 ] A 3D cell culture is important for sustaining the
structural and functional complexities of the cells, because
most in-vivo environments are 3D. Porous structures with
controllable porosity have benefi ts over scaffolds with random
pores, because they exhibit enhanced characteristics, such as
the ability to produce the proper nutrient supply, uniform cell
distribution, and high cell density.
Three-dimensional laser lithography offers excellent control
over the geometry and porosity of the sample, as well as high
resolution, and has been used recently to fabricate bio-scaf-
folds.
[ 30–33 ] In this technique, two laser beams are concentrated
to form a single ellipsoidal spot, which is used as a building
unit. The movement of a piezoelectric stage is controlled pre-
cisely to follow a pre-programmed path to partially expose the
photoresist. A full 3D structure can be produced after removing
the unexposed photoresist in a developer.
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The proposed microrobots have been designed by
determing the lateral distances between adjacent lines and
the line width of the microrobots by considering the size
of cells that would be placed inside the structure (generally
10–20 μ m). The design parameters and their measured values
are shown in Table 1 . The optimum laser power, scan speed,
and slice distance between scanning processes were defi ned
by testing the sample structures (see Figure S1, Supporting
Information). The appropriate writing speed and laser power
for reasonable feature quality depends on the minimum
bands of the designed structures. An overview of the fabrica-
tion process and scanning electron microscopy (SEM) images
of the fabricated microrobots are shown in Figure 1 . SU-8 was
used as a high contrast epoxy-based photoresist to provide the
mechanical stability required for complex, full 3D structures.
The fabricated structures were coated with Ni, which can be
magnetized and manipulated using magnetic fi elds. Finally,
the structures were coated with Ti, a non-toxic material, to
minimize cytotoxicity.
High saturation magnetization and low coercivity are
desired for microrobot movement. Figure 1 e shows the meas-
ured magnetization per unit volume for nickel using Physical
Property Measurement System (PPMS; Quantum Design,
US). The measured saturation magnetization per volume was
686 kA m
− 1 (686 emu cm
− 3 ) and the coercivity was 5 kA m
− 1
(62.83 Oe), which suggested that the deposited nickel has
a perfect ferromagnetic nature. The size of the microro-
bots affects their motion. Increasing the microrobot size
with a fi xed magnetic material volume would decrease the
velocity as the hydrodynamic drag force is increased. How-
ever, coating the structure with a greater volume of magnetic
material increases the driving force, while the drag force does
T a b l e 1 . Designed and measured microrobot sizes.
Design
(a)
[ μ m]
I (I ′ ) II (II ′ ) III (III ′ ) IV (IV ′ )
Length 153.98 144.20 154.40 156.60
(157.00)
(b) (147.20) (157.40) (159.60)
Diameter 78.00 73.00 73.00 73.00
(81.02) (76.00) (76.00) (76.00)
Line width 1.98 1.98 1.98 1.98
(5.08) (5.08) (5.08) (5.08)
Pore size 13.22 16.00 20.00 24.00
(10.20) (13.00) (17.00) (21.00)
(a) Each microrobot design has two shapes: cylindrical (I, II, III, and IV), and hexa-
hedral (I ′ , II ′ , III ′ , and IV ′ ). The diameter of the cylindrical shape of the microrobots
corresponds to the width or height of the hexahedral-shaped microrobots; (b) The
measured values for Type I were actually measured. The other values, Type I ′ , II,
II ′ , III, III ′ , IV, and IV ′ are the expected values based on the Type I measurement
(see Figure S2).
Figure 1 . a) Overview of the microrobot fabrication process. b) Scanning electron microscopy (SEM) image of the fabricated microrobots. c) Enlarged
SEM image of a cylindrical-shaped microrobot. d) Enlarged SEM image of a hexahedral-shaped microrobot. e) Magnetization of the microrobots per
unit volume of nickel.
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rotational motion (see Videos S1 and S2, Supporting Infor-
mation). The microrobots were controlled along complicated
trajectory lines to demonstrate synchronized swimming and
targeted control behaviors, as shown in Figures 2 e and f (see
Videos S3 and S4).
There are two resistive forces working against the motion of
the microrobot: the drag force and surface friction. For manipu-
lation, the input magnetic force must overcome these resistive
forces. A magnetic force in the z -direction was also required to
compensate for the weight of the microrobot. The translational
motion dynamics can be modeled as
Fm+Fr+Fg=mdv
dt
(3)
where F m
is the magnetic force, F r
is the resistive force
(including the surface friction and drag force), F g
is the gravita-
tional force, m is the mass, and v is the translational velocity of
the microrobot.
The microrobot was aligned with the z -axis by applying
an external magnetic fi eld along the same axis, as shown in
Figure 2 a. Magnetic torque can be calculated using Equation (1)
for rotational motion of the cylindrical microrobot as depicted in
Figure 2b. The magnetic forces for the two types of microrobot
were calculated using Equation (2) , as shown in Figure 3 a. The
driving magnetic force is proportional to the external magnetic
fi eld gradient and volume of nickel. Figure 3 b shows the mean
value of the translational velocity of the microrobots from fi ve
trials as a function of the magnitude of the applied magnetic
fi eld gradient. When an external fi eld gradient of 800 mT m
− 1
was applied in the x- direction, the translational velocity of the
microrobot was approximately 50 μ m s − 1 for the cylindrical
microrobot ( ≈ 1/3 body lengths per second). The results showed
not change signifi cantly. For example, doubling the magnetic
material thickness will roughly double the magnetic driving
force, while the drag force remains constant. A higher driving
force can also lead to better control over the microrobot. Rota-
tional and translational locomotion of the microrobot require a
magnetic torque and force on the magnetized structure.
[ 34–37 ]
The magnetic material on the surface of an anisotropic struc-
ture induces rotational motion, and the structure aligns with
the external magnetic fi eld ( B ) direction. Magnetic torque and
force can be calculated using the magnetic fi eld ( B ) and mag-
netic fi eld gradient (∇ B ) as follows:
Tm=VM×B (1)
Fm=V(M·∇)B (2)
where V is the volume of the magnetized object and M is the
uniform magnetization of the magnetic material.
The microrobot was manipulated using a customized mag-
netic actuation system (Minimag; Aeon Scientifi c, Switzerland).
In this system, the magnetic fi eld was generated by the linear
superposition of individual fi elds from eight coils carrying dif-
ferent currents.
[ 38 ] The microrobot was controlled in deionized
(DI) water in a plastic container, with fi ve degrees of freedom
(5-DOF): three translational ( x , y , and z ) and two rotational
(around the z - and x -axes) DOF. An external magnetic fi eld
was applied in the z -direction to align the principal axis of the
microrobot in the same direction, as shown in Figures 2 a and
c. Then, a gradient fi eld was used to translate the microrobot
along the x -axis direction. The maximum generated magnetic
fi eld was 800 mT m
− 1 . Figures 2 b and d show the rotation of
the microrobot with respect to the z- direction, with a rotation
frequency of 3 Hz. Figures 2 c and d show time-lapsed images
of the cylindrical microrobot undergoing translational and
Figure 2 . Schematic description of the a) translational motion and b) rotational motion of the cylindrical microrobot. Time-lapsed images of the
cylindrical microrobots c) translational motion (see Video S1) and d) rotational motion (see Video S2). e) Synchronized swimming with rolling motion
(see Video S3). f) Targeted control with rotational motion (see Video S4).
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hexahedral microrobot for the same magnetic fi eld gradient.
For the hexahedral microrobot, a nonlinear relationship was
evident between the translational velocity and the magnetic
fi eld gradient; this could be attributed to the nonlinear char-
acteristics of the velocity and resistive force. Since the drag
force is linear with respect to the velocity, the friction force
plays a greater role in the nonlinear character of the hexahe-
dral microrobot.
The surface area of the hexahedral microrobot was larger
than that of the cylindrical microrobot. Since Ni was deposited
uniformly on the surfaces of both microrobots, the hexahedral
microrobot had a larger volume of nickel. Therefore, the mag-
netic moment of the hexahedral microrobot was greater than
that of the cylindrical microrobot, which implies that a greater
magnetic force needed to be applied to the hexahedral micro-
robot for a specifi c magnetic fi eld gradient ( Equation (2) and
Figure 3 a). However, the hexahedral microrobot exhibited a
lower translational velocity, which might have been caused by
a higher resistive force. Therefore, the cylindrical microrobot
design is favorable for minimizing the resistive force against
manipulation.
In this study, HEK 293 cells were cultured inside porous
microrobots.
[ 39 ] Figure 4 shows SEM and confocal microscopy
images of the microrobots. The HEK 293 cells were affi xed
using paraformaldehyde solution, before SEM inspection, after
96 h of cell culture. Filopodia formed during cell migration, as
depicted in the enlarged SEM image (Figure 4 b), which indi-
cates that the cells interacted with the microrobots. The micro-
robots were coated with poly-
L -lysine (PLL) before cell culture.
PLL is a synthetic amino acid chain that is positively charged
and used widely as a coating material to enhance cell attach-
ment. In addition, PLL does not react in the staining assay.
Since the cell surfaces are negatively charged, cells attach to
the PLL via ionic bonding. Since PLL is a synthetic molecule,
it does not stimulate cells cultured on it biologically. There-
fore, we can consider the microrobot as a supporting structure
and PLL simply as a linking material for cells.
[ 40 ] The results
revealed that the microrobot material was not cytotoxic to the
myoblasts, as indicated by the ease in adhesion, migration,
and proliferation of the cells over the structure. The confocal
microscopy images were obtained after staining the cells inside
the microrobots.
In conclusion, we have demonstrated multifunctional micro-
robots for targeted cell delivery using 3D laser lithography. The
microrobots were coated with Ni and Ti layers as magnetic and
biocompatible materials, respectively. The fabricated porous 3D
structures were used for 3D cell cultures of HEK 293 cells. The
microrobots were controlled in a magnetic fi eld for targeted
transportation. The materials used for the structures were not
cytotoxic to myoblasts, as the cells readily adhered, migrated,
and proliferated over the structure. The optimum fabrication
parameters, established for the proposed microrobot structures,
can be easily customized for different cell types. Microrobots
with cylindrical and hexahedral shapes were manipulated in
DI water by applying an external magnetic fi eld gradient in
the x- direction when they were aligned with the z -axis. We
also have demonstrated more complicated trajectories of these
microrobots with the manipulator. This work has disclosed
the feasibility of the proposed porous microrobot as a 3D cell
a linear dependence of the required magnetic fi eld gradient on
the translational velocity for the cylindrical-shaped microrobots.
However, for the hexahedral-shaped microrobots, the relation-
ship between the translational velocity and input force was
nonlinear.
Since the Reynolds number was low under these experi-
mental conditions, we could consider the microrobot motion
to be quasi-static. For constant velocity motion in the x- direc-
tion, from Equation (3) , the magnetic and resistive forces are
balanced and there is no gravitational force in the horizontal
direction. The resistive force consists of the drag and friction
forces. The drag force is linearly dependent on the microrobot
velocity in a low-Reynolds number fl ow. Figure 3 b indicates
that a cylindrical microrobot has a higher velocity than a
Figure 3 . a) Calculated magnetic force on the microrobots, along with
their volume of nickel and magnetic fi eld gradient. b) Translational
velocity of the cylindrical and hexahedral microrobots in the x- direction
as a function of the applied magnetic fi eld gradient. The microrobots
were aligned with the z- direction. (Note that these data correspond to
Figures 2 a and c for the cylindrical robot.)
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magnetic manipulation, Jiyeon Park (DGIST) for assistance with the
SEM inspection, Eunjung Kim (Kyungbuk National University) for
suggestions regarding cell cultures, and Seungyeong Im (DGIST) for
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Note: The license of this manuscript was updated after initial online
publication.
Received: April 3, 2013
Revised: May 28, 2013
Published online: July 17, 2013
transportation system or drug delivery system, with targeted
micromanipulation for in-vivo applications.
Experimental Section
Microrobot fabrication : A 3 cm glass wafer was cleaned in an
ultrasonic bath, using isopropyl alcohol (IPA) to remove any residual
dust or organics. SU-8 (1.25 mL NANO SU-8 100, MicroChem, US) was
spin-coated onto the glass wafer in two steps: 500 rpm for 10 s with a
speed ramp of 100 rpm s
− 1 , and 1000 rpm for 30 s with a speed ramp
of 300 rpm s
− 1 . This produced a 100 μ m-thick layer of SU-8 on the glass
wafer surface. Then, the substrate was baked using a two-step process
at 65 ° C for 10 min, followed by 95 ° C for 30 min. Then, the substrate
was cooled to room temperature for 10 min. Two-photon polymerization
(TPP) and 3D laser lithography were conducted to polymerize the
designed structures partially, followed by a pre-development bake at
65 ° C for 1 min and a 95 ° C bake for 10 min. After cooling the substrate,
mr-Dev 600 (micro resist technology GmbH, Germany) was used to
develop the SU-8 for 20 min. To deposit a Ni/Ti bilayer on the polymer
microrobots, 150 nm of Ni was deposited as a magnetic material using
e-beam evaporation; the chuck was rotated and tilted to reduce the
shadowing effect. This was followed by deposition of a 20 nm-thick layer
of Ti to provide biocompatibility.
Supporting Information
Supporting Information is available from the Wiley Online Library or
from the author.
Acknowledgements
We thank the FIRST lab of ETH Zurich for technical support. The authors
are also grateful to Junman Lee (DGIST) for help with the microrobot
Figure 4 . a) SEM image of a hexahedral microrobot after cell culture and b) an enlarged SEM image. Filopodia are clearly shown in this enlarged image.
Confocal microscope images of the c) hexahedral and d) cylindrical microrobots after staining of the cells.
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