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Phan1,a 1 Department of Physics, University of South Florida, Tampa, Florida 33620, USA 2 Institute of Materials Science, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, C

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A highly sensitive magnetic biosensor for detection and quantification of anticancer

drugs tagged to superparamagnetic nanoparticles

J Devkota, J Wingo, T T T Mai, X P Nguyen, N T Huong, P Mukherjee, H Srikanth, and M H Phan

Citation: Journal of Applied Physics 115, 17B503 (2014); doi: 10.1063/1.4862395

View online: http://dx.doi.org/10.1063/1.4862395

View Table of Contents: http://scitation.aip.org/content/aip/journal/jap/115/17?ver=pdfcov

Published by the AIP Publishing

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A highly sensitive magnetic biosensor for detection and quantification

of anticancer drugs tagged to superparamagnetic nanoparticles

J Devkota,1J Wingo,1T T T Mai,2X P Nguyen,2N T Huong,3P Mukherjee,1

H Srikanth,1,a)and M H Phan1,a)

1

Department of Physics, University of South Florida, Tampa, Florida 33620, USA 2

Institute of Materials Science, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam

3

Department of Physics, Hanoi National University, 334 Nguyen Trai, Hanoi, Vietnam

(Presented 7 November 2013; received 23 September 2013; accepted 21 October 2013; published

online 17 January 2014)

We report on a highly sensitive magnetic biosensor based on the magneto-reactance (MX) effect of

a Co65Fe4Ni2Si15B14 amorphous ribbon with a nanohole-patterned surface for detection and

quantification of anticancer drugs (Curcumin) tagged to superparamagnetic (Fe3O4) nanoparticles

Fe3O4nanoparticles (mean size,10 nm) were first coated with Alginate, and Curcumin was then

tagged to the nanoparticles The detection and quantification of Curcumin were assessed by the

change in MX of the ribbon subject to varying concentrations of the Fe3O4nanoparticles to which

Curcumin was tagged A high capacity of the MX-based biosensor in quantitative analysis of

Curcumin-loaded Fe3O4nanoparticles was achieved in the range of 0–50 ng/ml, beyond which the

detection sensitivity of the sensor remained unchanged The detection sensitivity of the biosensor

reached an extremely high value of 30%, which is about 4–5 times higher than that of a

magneto-impedance (MI) based biosensor This biosensor is well suited for detection of

low-concentration magnetic biomarkers in biological systems.V C 2014 AIP Publishing LLC

[http://dx.doi.org/10.1063/1.4862395]

A combination of magnetic sensors with functionalized

magnetic nanoparticles offers a promising approach for a

highly sensitive, simple, and quick detection of cancer cells

and biomolecules.13 This method provides several

advan-tages over conventional optical and electrochemical

techni-ques.2 However, a precise detection of small amounts of

cancer cells that have taken up magnetic nanoparticles or

biomolecules/anticancer drugs attached to magnetic

nanopar-ticles in real biological systems is a challenging task and

requires magnetic sensors with improved sensitivity.3

Recently, particular attention has been paid to the

devel-opment of a new class of magnetic biosensor based on the

giant magneto-impedance (GMI) effect, because of its high

detection sensitivity achieved at ambient temperature.411

GMI sensors are also cost-effective, power-efficient, reliable,

quick-response, and portable.4 Basically, GMI is a large

change in the ac impedance (Z¼ R þ jX, where R and X are

ac resistance and reactance, respectively;j is imaginary unit)

of a ferromagnetic conductor subject to a dc magnetic field.9

Since GMI often occurs at high frequencies (f > 1 MHz),

where the skin effect is significant enough to confine the ac

current to a sheath close to the surface of the conductor, it is

very sensitive to change in near-surface magnetic signals

Therefore, it is possible to detect various concentrations of

magnetic nanoparticle-based biomarkers in biological

sys-tems by evaluating the change in GMI of a soft

ferromag-netic amorphous ribbon due to the fringe fields of the

nanoparticles located on the surface of the ribbon.9,11A large

body of work has been performed to prove the usefulness of this biosensing technique.411For instance, Yanget al have successfully developed a GMI-based microchannel system for quick and parallel genotyping of human papilloma virus type 16/18 and for targeted detection of gastric cancer cells.6,7 While previous efforts were devoted mainly to developing magnetic biosensors based on the GMI effect which have limited detection sensitivities (5–10%),4 8we have recently shown that by exploiting the real and imagi-nary components of GMI, namely, the ac magneto-resistance (MR) and magneto-reactance (MX) effects, it is possible to improve the detection sensitivity of the biosensor by up to 50% and 100%, respectively.9The MX-based sensor shows the most sensitive detection of superparamagnetic nanopar-ticles (mean size,10 nm) at low concentrations In effort to further improve the detection sensitivity of this biosensor,

we have recently developed a method of patterning nano-holes onto the surface of a ribbon with the use of an appro-priate concentration of HNO3 acid.10 We have shown that the presence of nanoholes on the surface of the ribbon improves the detection sensitivity of the sensor significantly

In this work, we show the high capacity of using a

MX biosensor for detection and quantification of anticancer drug Curcumin (Cur) tagged to superparamagnetic (Fe3O4) nanoparticles via bio-functionalized nanoconjugates (Fe3O4-Alg-Cur), where Alginate (Alg) was used to chemi-cally stabilize the surface of Fe3O4 nanoparticles Since

Fe3O4nanoparticles are widely used as magnetic resonance imaging (MRI) contrast agents, our biosensing technique can also be used as a new, low-cost, fast and easy pre-detection method before MRI

a) Authors to whom correspondence should be addressed Electronic

addresses: sharihar@usf.edu and phanm@usf.edu.

JOURNAL OF APPLIED PHYSICS 115, 17B503 (2014)

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Fe3O4 nanoparticles of 10 6 2.5 nm diameter were

chemically stabilized by coating with Alg (which is a

poly-saccharide extracted from brown algae), then functionalized

with Cur (which is a yellow compound isolated from

rhi-zome ofCurcuma longa L plant and is widely used as an

anticancer drug for applications in drug delivery and

hyper-thermia) to obtain the Fe3O4-Alg-Cur nanoparticles of

120 6 15 nm diameter The detail of the synthesis of these

functionalized nanoparticles has been reported elsewhere.11

The inset of Fig 1 shows a typical SEM image of the

Fe3O4-Alg-Cur nanoparticles The room-temperature

super-paramagnetic nature of the Fe3O4-Alg-Cur nanoparticles is

evident with the absence of the coercivity (HC 0) in the

magnetic hysteresis M(H) loop taken at 300 K and the best

fit of the M(H) data to the Langevin function.11

To perform experiments to detect Fe3O4-Alg-Cur

nano-particles, a biosensor prototype was designed using a

com-mercial Co65Fe4Ni2Si15B14 amorphous ribbon (MatglasV R

2714A) of dimension 16 mm 2 mm  0.015 mm as a

mag-netic sensing element The sensing region of the ribbon

sur-face was treated with 5 ll of17 vol % HNO3, then rinsed

with DI water after 24 h with the water molecules on the

rib-bon surface to be allowed to evaporate naturally at room

temperature Changes in MX of the ribbon before and after

drop-casting Fe3O4-Alg-Cur nanoparticles with various

con-centrations on the ribbon surface were recorded over a

rib-bon length of 10 mm using an HP4192A impedance analyzer

at a fixed ac current of 5 mA and in axial dc magnetic fields

of up to 6120 Oe The MX ratio and detection sensitivityðgÞ

for a given frequency were defined and calculated as

DX

X ¼X Hð Þ  XðHmaxÞ

XðHmaxÞ  100%; (1) and

g¼ ½MXmax; MNP ½MXmax; PR; (2)

where½MXmax ¼ DX

X

h i max is the maximum value of the MX ratio given in Eq.(1) MNP and PR stand for magnetic

nano-particles and plain ribbon, respectively

Figure2(a)shows the magnetic field dependence of the

MX ratio (DX/X) taken at 0.5 MHz for a plain ribbon, with

10 ll of DI water, 10 ll of a 250 ng/ml Fe3O4-Alg-Cur nano-particle solution and after removing the solution completely For all the samples the MX curves show a double-peak fea-ture (see, inset of Fig.2(a)), due to the presence of transverse magnetic anisotropy in a Co-based amorphous ribbon.911 The presence of water and Fe3O4-Alg-Cur nanoparticles on the surface of the ribbon has negligible influence on the double-peak structure of the DX/X profile The presence of water (with and without dispersed Fe3O4-Alg-Cur nanopar-ticles) does also not alter the DX/X ratio of the plain ribbon, indicating a negligible corrosion effect of water on the pres-ently used ribbon It is worth noting here that the presence of

Fe3O4-Alg-Cur nanoparticles on the surface of the ribbon results in an increase in the DX/X ratio by 18% This increase in the MX ratio can be explained by considering the effect of the fringe fields of Fe3O4-Alg-Cur nanoparticles on the superposition of the applied axial dc magnetic field and the induced transverse ac field (due to an ac current flowing along the axis of the ribbon).9,11

To probe the effects of water and Fe3O4-Alg-Cur nano-particles on the MX response of the ribbon at different frequencies, we have measured the MX of the plain ribbon, with water (10 ll), and with 10 ll of a 250 ng/ml

FIG 1 Magnetic hysteresis loop of the Fe 3 O 4 -Alg-Cur nanoparticles The

inset shows a typical SEM image of the Fe 3 O 4 -Alg-Cur nanoparticles.

FIG 2 (a) Magnetic field dependence of the MX ratio (DX/X) at 0.5 MHz for the plain ribbon, with water (10 ll), with 10 ll of a 250 ng/ml

Fe 3 O 4 -Alg-Cur nanoparticle solution, and after removing the solution The inset shows an enlarged view of the DX/X profiles; (b) Frequency depend-ence of the maximum MX ratio ([DX/X] max ) for these samples The inset shows the frequency dependence of the sensor detection sensitivity (g) as calculated using Eq (2)

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Fe3O4-Alg-Cur nanoparticle solution over a frequency range

of 0.2–2.5 MHz Figure 2(b) shows the frequency

depend-ence of maximum MX ratio (i.e., [DX/X]max) for these

sam-ples [DX/X]max is largest at 0.2 MHz and decreases sharply

with increasing frequency in the range of 0.2–2.5 MHz

From a biosensing perspective, it is interesting to highlight

that while almost identical values of [DX/X]maxare obtained

for the plain ribbon with and without water, the presence of

Fe3O4-Alg-Cur nanoparticles results in significantly larger

values of [DX/X]maxin the frequency range of 0.2–2.5 MHz

We have defined the detection sensitivity of the sensor (g),

using Eq (2), as the difference in [DX/X]max between the

plain ribbon and the ribbon with Fe3O4-Alg-Cur

nanopar-ticles The variation in g with frequency is plotted in inset of

Fig.2(b) As one can see in this figure, g has a maximum

value of 30% at 0.2 MHz and decreases sharply with

increase in the frequency This value of g is about 4–5 times

higher than that of a GMI-based biosensor reported in the

literature.411 For this reason, a frequency of 0.2 MHz was

chosen for studies of detection of Fe3O4-Alg-Cur nanopar-ticles of varying concentrations

Figure 3(a) displays the magnetic field dependence of the MX ratio at 0.2 MHz for the ribbon with Fe3O4-Alg-Cur nanoparticles at various concentrations Using Eq (2), the detection sensitivity (g) has been calculated for all particle concentrations, and its variation with particle concentration

is depicted in Fig.3(b) It can be seen that g first increases sharply in the range of 0–50 ng/ml (from3.5% for 10 ng/ml

to30% for 50 ng/ml) and then remains almost unchanged for higher concentrations (50 ng/ml–250 ng/ml) A similar trend has recently been reported and explained in detail by

us for the case of non-functionalized Fe3O4nanoparticles.9

In summary, we have demonstrated the possibility of using the magneto-reactance effect of a soft ferromagnetic amor-phous ribbon with a nanohole-patterned surface to develop a highly sensitive magnetic biosensor for detection and quantifi-cation of anticancer drugs tagged to superparamagnetic nanoparticles

The research at USF was supported by the Florida Cluster for Advanced Smart Sensor Technologies and by USAMRMC through Grant Nos W81XWH-07-1-0708 and W81XWH1020101/3349 The research at IMS-VAST was supported by the National Foundation for Science and Technology Development of Vietnam through Grant No 103.02-2011.31 (NXP) The research at HUS was supported

by the National Foundation for Science and Technology Development of Vietnam through Grant No 103.02-2012.69 (NTH)

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FIG 3 (a) Magnetic field dependence of the MX ratio (DX/X) at 0.2 MHz

for various concentrations of Fe 3 O 4 -Alg-Cur; (b) Particle concentration

de-pendence of the sensor’s detection sensitivity.

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