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Localized catalysis driven by the induction heating

Cite this: DOI: 10.1039/d0cy00439a
of magnetic nanoparticles†
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Sarah R. Yassine, Zaynab Fatfat, Ghinwa H. Darwish and Pierre Karam *

Received 5th March 2020,
Accepted 19th May 2020
DOI: 10.1039/d0cy00439a
rsc.li/catalysis
Controlling temperature with high spatial resolution has been a challenge and the bottleneck for advancing
scientific discoveries at the micro-scale level. Herein, we exploit the heat generated from magnetic
nanoparticles when placed in an alternating magnetic field to drive catalytic chemical reactions. A catalytic
microstructure was assembled using a positively charged polyelectrolyte in the presence of negatively
charged magnetic and gold nanoparticles. As a proof of concept, we monitored the conversion of
resazurin into the fluorescent resorufin in solution and when confined in small hydrogels. In both cases, we
demonstrate the possibility to drive chemical reactions using the locally generated heat from magnetic
nanoparticles. This might prove an effective strategy for energy efficient catalysis.

1. Introduction resolution. This ability will have a tremendous effect on how

In this manuscript, we demonstrate the possibility to drive
chemical reactions using localized heat generated from
magnetic nanoparticles.
Temperature is a fundamental physical parameter that
controls chemical, physical, and biological reactions.1–3
While the science of the 21st century focuses on unraveling
phenomena at the sub-micron level, temperature is still being
applied using large heat sources relative to the size of the
system of interest. The lack of available methods to
accurately manipulate and measure the temperature at the
micro-scale has limited the advancement of both
fundamental studies and small technologies.4–11 For
instance, cellular and even sub-cellular thermal processes are
studied using temperature-controlled chambers or heated
glass coverslips which lead to a non-homogenous thermal
distribution.12–14 Thermally activated pro-drugs are yet
another example where micro-particle degradation is studied
and optimized in large reaction volumes.15–17 While these
two examples are commonly reported in the literature, many
more examples could be cited from the different fields of
science and engineering.18,19 There is, therefore, a pressing
need to deliberately generate heat with exquisite spatial
Chemistry Department, American University of Beirut, P. O. Box 11-0236, Riad El-
Solh, 1107 2020, Beirut, Lebanon. E-mail: pierre.karam@aub.edu.lb;
Fax: +961 1365217
† Electronic supplementary information (ESI) available. See DOI: 10.1039/
d0cy00439a
we perform and understand chemical and biological
processes at the sub-micron scale.
Gold nanoparticles (AuNPs) can be plasmonically heated
upon light excitation to enhance catalytic reactions of either
the gold particle itself or when coupled to other metallic
surfaces.20,21 Scaiano et al. reported the photocatalytic
reduction of resazurin using the local heat generated from
the plasmonic excitation of gold nanoparticles.22 This
approach, however promising, might be limited for two
reasons: (1) the high laser power needed to excite the gold
nanoparticles can be disruptive to many organic matrices, in
general, and living organs in particular, and (2) the
penetration depth of visible and near-IR light sources is
limited in opaque or semi-transparent materials. Magnetic
nanoparticles (MNPs), on the other hand, generate heat when
placed in an alternating magnetic field while presenting no
harm to organic matrices and have large penetration depth
in a wide range of materials (organic and inorganic matrices,
human tissues, etc.).23–28 These particles have been, for
instance, exploited in new therapeutic strategies against
cancer. Once they accumulate in a tumor, the localized heat
induces apoptosis.29,30 Despite the stated advantages, the
scope of work where MNPs are currently used is still
somewhat limited.
Herein, as a proof of concept, the heat generated by the
magnetic particles is used to catalyze the reduction
conversion of resazurin to the highly fluorescent product
resorufin in the presence of NH2OH (Fig. 1). Using this
strategy, we were able to drive the aforementioned chemical
reaction at a similar efficiency to the one performed in a water
bath under the same experimental conditions. We chose this

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Fig. 1 (A) The catalytic reduction reaction of resazurin to the fluorescent resorufin in the presence of iron oxide (Fe3O4), gold nanoparticles
(AuNPs), and the reducing agent NH2OH. (B) Schematic representation of the heat induction setup; a frequency generator is connected to a coil
where the micro-catalytic MNPs/AuNPs solution is placed and subjected to an alternating magnetic field (frequency = 110 kHz). (C) The assembly
of the prepared micro-catalytic MNPs/AuNPs structure is driven by the electrostatic interaction between negatively charged MNPs and AuNPs
using positively charged polyelectrolytes (PDDA).

reaction since it is easy to monitor the formation of its
product using steady-state fluorescent spectroscopy.
2. Results and discussions
The preparation of the catalytic microstructure (MNPs/
AuNPs) is achieved by first synthesizing citrate-capped
magnetic iron oxide nanoparticles (140 mg mL−1; 33 ± 8 nm
N = 132) and gold nanoparticles (1.4 mg mL−1; 24 ± 6 nm N =
154), (Fig. 2) followed by the addition of the positively
charged polyelectrolyte (poly diallyl dimethyl ammonium
chloride (PDDA)) to a mixture of equal volumes of MNPs and
Au NPs.
In order to confirm the assembly, an external magnetic
field was applied to the MNPs/AuNPs mixture, and the
absorption spectrum of the resulting supernatant was
compared to that of a pristine gold nanoparticles solution.
The absence of any detectable signal representing gold
nanoparticles in the supernatant indicates the efficient
assembly of the metal particles onto the pulled MNPs
(Fig. 3A and B). In addition, dynamic light scattering
measurements showed an increase in the average
hydrodynamic radius from 92 nm and 257 nm for gold and
iron oxide nanoparticles, respectively, to 3800 nm upon the
addition of PDDA (Table S1†). Finally, TEM images of the
catalytic complex revealed large aggregates. However, these
images were not conclusive given the size distribution of the
Au and MNP particles and the difficulty in comparing their
contrast given the aggregated state of the sample (Fig. 3C).
To evaluate the reaction efficiency, we monitored the
fluorescence intensity of resorufin produced under different
experimental conditions at different time points. The choice
of concentrations of both nanoparticles took into
consideration not only the conversion efficiency but also the
technical aspect of the experiment such as avoiding large
aggregates, signal scattering, or quenching of the fluorescent
signal by the gold nanoparticles. The reaction temperature
was controlled by placing the solution in a water bath. The
optimized solution was then tested at different temperatures
ranging between 25.0 °C and 85.0 °C with a step increment
of 10.0 °C (Fig. S4†). The temperature was monitored and
tracked using a thermocouple dipped inside the solution and
connected to a data logger. As such, we carried all further
catalytic reactions at 45.0 °C. At this temperature, the
reaction kinetics would allow us to observe the enhancement,
if any, in the conversion of resazurin when carried out in a

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Fig. 2 TEM images and size distribution for (A) magnetic nanoparticles (MNPs) (33 ± 8 nm N = 132) and (B) gold nanoparticles (AuNPs) (24 ± 6 nm
N = 154).
water bath and compare it to that placed in an alternating
magnetic field.
To ensure comparable experimental conditions
throughout the experiment, the solution temperature was
monitored over time. Within the first 2–3 minutes, in both
solutions, the target temperature (45.0 °C) was achieved and
remained stable during the entire experiment window (Fig.
S5†). At different time intervals, the fluorescent signal of the
resorufin was sampled and compared. The catalytic micro-
structure when placed in an alternating magnetic field
showed a comparable catalytic conversation to the water bath
solution (Fig. 4). While all trials consistently followed the
same trend, the measured fluorescent signal varied from one
sample to another (evident by the large error bars in Fig. 4).
The micro-catalytic structure has a tendency to aggregate in
solution. Despite taking many measures to homogenize the
solution before making any transfer to the reaction mixture,
we believe our effort did not lead to completely eliminating
this error.
While both experimental heating conditions yielded
similar efficiency, the localized heat method could be utilized
to manipulate chemical reactions and synthesize molecules
with deliberate spatial accuracy. In addition, the locally
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generated heat provides a more energy-efficient option. An
external heating sources is relatively sluggish method for
transferring energy into the catalytic hotspot site, since it
depends on the thermal conductivity of the reactor. The local
heat can reduce the rate of side products.
There has been growing evidence that indicates that the
local surface temperature of the nanoparticles is higher than
the solution temperature which can allow an efficient
conversion. Pellegrino et al., for instance, probed the
distance-dependent temperature as generated by magnetic
nanoparticles using a thermo-sensitive molecule.31 The local
temperature surrounding the MNPs was found to be
approximately 45 °C greater than the solution temperature.
Zink et al. also reported a temperature gradient with a
measured MNPs surface temperature of 42 °C while the
solution temperature was equal to 19 °C.32 In another
example, the localized heat was used to increase in the total
negative charge of the silica surface due to the deprotonation
of silanol groups.33 CO2 hydrogenation was also performed
by locally generated heat.34 Despite gold nanoparticles being
widely reported as an efficient catalyst for the reduction of
resazurin,22,35,36 we observed a substantial catalytic activity
from the magnetic nanoparticles alone. This activity was
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Fig. 3 (A) The assembly of the micro-catalytic structure was evident by the clear supernatant upon applying an external magnetic field. (B)
Absorption spectra of pristine gold NPs solution and of the supernatant of a MNPs/AuNPs sample upon separation. (C) TEM images of MNPs/
AuNPs catalytic complex at different scales.

estimated to be around 80% (Fig. 5). Iron oxide has been

reported as a catalyst for many chemical reactions such as
the oxidation of carbon monoxide,37 the production of lower
olefins,38 and the decomposition of hydrogen peroxide.39

Fig. 4 Comparison between the fluorescence intensities of resorufin

produced by the catalytic reduction of resazurin when heated by an
external heat source (■) to that by the micro-catalytic MNPs/AuNPs
structure in an alternating magnetic field (●) at different time intervals.
The histograms represent the average fluorescent value of 5
independent trials at 30 min. Error bars were calculated from the Fig. 5 Comparison between the fluorescence intensities of resorufin
standard deviations of the 5 independent measurements. The solution produced by the catalytic reduction of resazurin heated by induction
temperature in both conditions was maintained at 45.0 °C. The lines using only magnetic nanoparticles to that by a mixture of magnetic
connecting the experimental points are for visual aid. and gold nanoparticles.

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Fig. 6 Recyclability of the MNPs/AuNPs complex tested over three
cycles. The different histograms represent the fluorescence intensities
of resorufin acquired after 45 min using the same micro catalytic
sample structure.
To monitor the long-term stability of the micro-catalytic
system, we recycled the MNPs/AuNPs particles three times. At
the end of each cycle, the particles were collected washed
multiple times and re-suspended in a fresh solution of
resazurin. The conversion was monitored as previously
reported. The three cycles showed similar efficiency at
different time intervals (Fig. 6 and S7†).
Based on these promising findings, we argued that these
localized catalytic reactions would allow the deliberate
production of molecules of interests in a spatially confined
micro-volume even when a small amount of the micro-
catalytic structure is introduced. Hydrogels have been used in
chemistry and biology to mimic soft matrices including but
not limited to the extracellular medium.40,41 Motivated by
this fact, we checked if it is possible to catalyze chemical
reactions in small localized volumes in soft materials. The
success in achieving this could translate, in the future,
toward an in situ drug generation, for instance.42 For this
purpose, a thin agar gel layer containing resazurin was
prepared on a microscope slide. A few microliters of the
micro-catalytic mixed with NH2OH were introduced to the gel
Fig. 7 Fluorescent microscopy images of agar gel before and after exposure to an alternating magnetic field in the presence of resazurin, NH2OH,
and MNPs/AuNPs complex. The histograms represent the numerical values of the integrated fluorescence intensity before and after heat
induction. Images were acquired using a 5× objective with NA = 0.8 coupled with an excitation filter of 541–551 nm, and the emission was
collected between 565–605 nm.
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using a sharp needle. Fluorescent images were then acquired
before and after exposure to an alternating magnetic field,
under the same conditions, and quantified based on their
intensities (Fig. 7 and S8†). The integrated intensity obtained
after the gel exposure to an alternating magnetic field
showed an increase in its value between 100 and 150%. The
observed range of increased fluorescence intensity of the
different trials (Fig. S8†) might be the result of the variable
amount of the micro-catalytic structures introduced to the
gel. This experiment illustrates the possibility to drive
chemical reactions at the core of an organic matrix using
deliberately generated heat. The hydrogel could be
substituted with an organ and resazurin for a prodrug.
3. Conclusion
In conclusion, we successfully report the use of heat
generated at the microscale to drive the reduction conversion
of resazurin into the highly fluorescent product, resorufin.
This proof-of-concept experiment will eventually pave the way
for thermally control reactions with a high spatial resolution,
which would allow, for instance, the production of drugs with
surgical precision. Prodrugs, such as endoperoxides for
example, could be delivered to the organs of interest while
their catalyzing uncaging upon local heating to release
reactive oxygen species intracellularly with surgical spatial
control. Molecular printing, nanofabrication, or even local
molecular enrichment are just some of the many applications
that one might contemplate. The current reported
nanoparticle complex could be improved if the magnetic
nanoparticles is dopped to increase is hyperthermia
efficiency.
4. Materials and methods
Materials
Resazurin sodium salt, goldIJIII) chloride trihydrate, ironIJIII)
chloride hexahydrate, ironIJII) chloride tetrahydrate,
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polyIJdiallyl dimethylammonium chloride) (PDDA), and
trisodium citrate dihydrate were purchased from Sigma
Aldrich. Hydroxylamine hydrochloride and ammonium
hydroxide (28%) were purchased from Acros. Difco LB agar
Lennox was obtained from BD Diagnostic.
Synthesis of iron oxide magnetic nanoparticles (MNPs)
Iron oxide magnetic nanoparticles (MNPs) were synthesized
using a previously published procedure.43 Briefly, equimolar
masses of ironIJII) chloride FeCl2·4H2O (1.2 g) and ironIJIII)
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chloride FeCl3·6H2O (3.25 g) were dissolved in 80 mL
deionized water. Next, 10 mL of ammonium hydroxide
solution (28% w/v) was added while mechanical stirring.
Twenty minutes later, 4.4 g of trisodium citrate dihydrate
powder was dissolved and the whole mixture was stirred
while the temperature was raised and maintained at 90 °C
for 30 min. After cooling down to room temperature, the
magnetic nanoparticles produced were collected by an
external magnet and re-suspended in 10 mL deionized water
(Fig. S1†) yielding an estimated 140 mg mL−1 solution of
particle size equal to ca. 257 nm (Table S1†).
Synthesis of gold nanoparticles (AuNPs)
The gold nanoparticles (AuNPs) were prepared following the
sodium citrate reduction method.44 In short, 80 μL of a 0.2 g
mL−1 goldIJIII) chloride trihydrate (HAuCl4·3H2O) solution was
diluted in 10 mL deionized water and stirred till boiling.
Then, 1.5 mL of 3% trisodium citrate dihydrate was added to
form a momentarily colorless solution that rapidly turns into
wine-red. The gold's concentration in the resulting
suspension was estimated to be 1.4 mg mL−1 (1.8 nM).
Gold-magnetic nanoparticle catalytic micro-catalytic structure
The assembly of the catalytic micro-structure was achieved by
the addition of a positively charged polyelectrolyte :
polyIJdiallyl dimethyl ammonium chloride) – PDDA – to a
mixture of 1 : 1 Fe3O4 : Au NPs by volume, followed by
vortexing for 15 min. This resulted in the assembly of MNPs/
AuNPs macro structures with the heat generating element
and the catalytic surface closely positioned. The
nanoparticles ratio provided enough magnetic nanoparticle
to raise the solution temperature within few minutes of the
start of the experiment. Also, the gold nanoparticles were
within the previously reported concentration range to allow
efficient catalytic conversion of rezasurin.22
Characterization of nanoparticles
Transmission electron microscope. TEM imaging of the
NPs was captured using a Hitachi H7600 transmission
electron microscope. The samples were imaged at an
accelerating voltage of 80 kV. The samples were prepared by
drop-casting 5-fold diluted solution on copper TEM grids
(TED Pella, 300 mesh) and allowing the samples to dry
overnight.
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Absorption spectra. Absorption spectra were measured
using Jasco, V-570 UV/VIS/NIR spectrophotometer in a double
beam mode. All solutions were placed in a 1 cm × 1 cm
quartz cuvettes while keeping the total volume constant and
equal to 2 mL. Before each measurement, the solution was
allowed to homogenize and stabilize for 2–3 min.
Steady-state fluorescent spectroscopy
Resazurin is a weak fluorescent blue dye that is widely used
in biological applications.22,32 Upon heating and in the
presence of AuNP as a catalyst and the reducing agent
hydroxylamine (NH2OH), resazurin is reduced into resorufin,
a strong fluorescence molecule. The reduction of resazurin
was done in a 2 mL-tube containing a mixture of 70 mg mL−1
MNPs/0.7 mg mL−1 AuNP, and 2 mM resazurin. Fluorescence
intensity of resorufin was obtained by first diluting the
reaction mixture in a 0.5 mM NaOH. All solutions were
placed in a 1 cm × 1 cm quartz cuvettes. Before each
measurement, the solution was allowed to homogenize and
stabilize for 2–3 min. Steady-state fluorescent spectroscopy
was acquired by exciting at 532 nm using a Thermo Scientific
Lumina spectrophotometer while collecting the emissions
between 545 nm and 700 nm.
Thermal heating of magnetic nanoparticles – MagneTherm
MagneTherm was used to generate an alternating magnetic
field using a built-in-coil NAN201003 at a 109.6 kHz. Initially,
the voltage was increased to its maximum value that is equal
to 32 V. Once the solution temperature reached 45 °C, the
voltage was adjusted manually and monitored down to
approximately 10 V to keep the solution thermally constant.
Temperature tracking
To insure comparable experimental conditions and maintain
a stable temperature, the thermal variations were measured
and tracked using the OAKTON WD-08516-83 FEP
thermocouple, dipped in the solution and connected to a
data-logger machine. Adjustments were manually introduced,
when needed, to maintain a constant value. Fig. S5† shows
an example of thermal tracking. Both solutions reached
steady values within the first few minutes and remained
relatively constant throughout the experiment.
Conflicts of interest
There are no conflicts to declare.
Acknowledgements
This work was supported by the University Research Board
(#103603) and the Collaborative Research Stimulus at the
American University of Beirut (#103320). The authors are also
thankful for the Kamal A. Shair Central Research Science Lab
(KAS CRSL) of the Faculty of Arts and Sciences at AUB for
providing access to their facilities.
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