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B3056 Journal of The Electrochemical Society, 164 (5) B3056 B3058 (2017) JES FOCUS ISSUE ON BIOSENSORS AND MICRO NANO FABRICATED ELECTROMECHANICAL SYSTEMS Communication—Accessing Stability of Oxidase[.]

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B3056 Journal of The Electrochemical Society, 164 (5) B3056-B3058 (2017)

JES FOCUS ISSUE ON BIOSENSORS AND MICRO-NANO FABRICATED ELECTROMECHANICAL SYSTEMS

Communication—Accessing Stability of Oxidase-Based Biosensors via Stabilizing the Advanced H2O2 Transducer

Elena V Karpova, Elena E Karyakina, and Arkady A Karyakin z

Chemistry Faculty of M V Lomonosov Moscow State University, 119991 Moscow, Russia

Operational stability of biosensors is of particular importance especially for wearable devices Prussian Blue (PB) based advanced

hydrogen peroxide transducer, 1000 times more active and selective than platinum, is deposited onto screen-printed structures and

stabilized with nickel hexacyanoferrate (NiHCF), both in open circuit mode Operational stability of PB-NiHCF bilayer based

biosensors and labile lactate oxidase is significantly improved in terms of twice longer half inactivation and ≈3.5 times lower

inactivation constant The dynamic range of PB-NiHCF based biosensors is similar to it for conventional PB based ones, which

allows using the former for similar purposes drastically improving their performance characteristics.

© The Author(s) 2017 Published by ECS This is an open access article distributed under the terms of the Creative Commons

Attribution 4.0 License (CC BY, http://creativecommons.org/licenses/by/4.0/ ), which permits unrestricted reuse of the work in any

medium, provided the original work is properly cited [DOI: 10.1149/2.0091705jes ] All rights reserved.

Manuscript submitted October 12, 2016; revised manuscript received December 27, 2016 Published January 18, 2017.This paper

is part of the JES Focus Issue on Biosensors and Micro-Nano Fabricated Electromechanical Systems.

Biosensors after their discovery1 , 2have found wide practical

ap-plications in various areas of human life The biosensor market is still

growing: from 5 billion $ in 20053to 15 billion $ in 2013.4Current

trend in clinical diagnostics as well as sports medicine is

continu-ous monitoring of metabolites Accordingly, varicontinu-ous biosensor based

wearable devices are elaborated requiring high operational stability

of the biosensors

Oxidases serve as terminal ones for more than 90% of enzyme

based biosensors As shown already in 70-s, the most progressive way

to couple the oxidase-catalyzed and the electrochemical reactions

allowing to achieve the lowest detection limit is to detect hydrogen

peroxide (H2O2), their side product.5 However, H2O2 oxidation on

platinum electrodes most widely used nowadays suffers from parasitic

signal produced by easily oxidizable compounds

More than 20 years ago we discovered Prussian Blue (iron

hexa-cyanoferrate) as selective electrocatalyst for hydrogen peroxide

reduc-tion allowing its low-potential detecreduc-tion in the presence of oxygen.6 , 7

In neutral aqueous media, favorable for applications in life science

and for biosensors, Prussian Blue (PB) is three orders of magnitude

more active, and three orders of magnitude more selective compared

to the commonly used platinum.8Nano-structuring the electrocatalyst

onto an inert electrode supports results in elaboration of the

electro-chemical sensor with record performance characteristics.9 , 10Despite

a number of non-iron transition metal hexacyanoferrates were also

proposed as suitable transducers for oxidase-based biosensors, these

materials are catalytically inactive; their apparent catalytic activity in

H2O2reduction is due to the presence of Prussian Blue as defects in

their structure.11

Combining novel enzyme immobilization protocols with

appar-ently the best electrocatalyst for H2O2reduction, the advanced

biosen-sors for glucose, glutamate, lactate have been elaborated.12 – 15Among

advantages of the PB based biosensors is their applicability for

wear-able devices, for example, for monitoring of undiluted sweat.15 We

note that the use of noble metals including platinum for analysis of

sweat is impossible because this excreted liquid contains various

pep-tides irreversibly inactivating these electrocatalysts

Main efforts for improvement stability of the biosensors were

de-voted to stabilization of the enzymes, the generally accepted ‘weak’

elements in biosensors However, the electrocatalyst upon action

(in-cluding Prussian Blue16) is also able to degrade We report that

opera-tion stability of the Prussian Blue based biosensors is also determined

by stability of the electrocatalyst Stabilizing the latter it is possible

to significantly prolong the biosensor lifetime

z E-mail: aak@analyt.chem.msu.ru

Experimental

Experiments were carried out with Millipore Milli-Q water All inorganic salts were obtained at the highest purity from Reachim (Moscow, Russia) and used as received D-Glucose was purchased from ICN Biomedicals, USA Sodium lactate, 40% solution, was

pur-chased from ICN Glucose oxidase (EC 1.1.3.4) from Aspergillus

niger (lyophilized powder, activity 270 IU) was purchased from

Sigma, Germany Lactate oxidase (EC 1.1.3.2) from Pediococcus sp.

(lyophilized powder, activity 72 IU) was from Sorachim, Switzerland Planar 3-electrode structures made by screen-printing (Rusens Ltd, Russia) contained carbon working electrode (Ø= 1.8 mm) PalmSens potentiostat (Netherlands) interfaced to PC was used

Interfacial synthesis of Prussian Blue was made by dipping a droplet of 2–4 mM K3[Fe(CN)6] and 2–4mM FeCl3 in 0.1 M HCl and 0.1 M KCl and initiating by addition of H2O2to a final concen-tration of 50–200 mM Deposition of Nickel Hexacyanoferrate was made using 0.5 M KCl and 0.1 M HCl as a background electrolyte Concentration of precursors (Ni2+, [Fe(CN)6]3−) was varied in the range 0.5–2 mM After deposition modified electrodes were annealed

at 100◦C during 1 h

Biosensors were made casting an enzyme containing drop (2μL) onto the transducer surface with subsequent drying at a room tem-perature for one hour Glucose oxidase casting mixture was pre-pared suspending aqueous enzyme (10 mg/mL) by 0.3% Nafion ana-logue in 85% isopropanol Lactate oxidase was suspended by 2% γ-aminopropyltriethoxysilane in 90% isopropanol

Results and Discussion

Among a number of approaches used for stabilization of Prussian Blue: covering with organic polymers,17 , 18entrapment in sol-gel19 – 21

or conductive polymer matrixes22 , 23 – building of multilayers with non-iron hexacyanoferrates isostructural to Prussian Blue seems to be the most progressive.24

We already reported on the open circuit interfacial deposition

of Prussian Blue22 allowing to avoid electrochemical techniques, highly required for cost-effective mass production In contrast to,22 we’ve chosen hydrogen peroxide as a reductant for ferric-ferrocyanide ([FeFe(CN)6]) complex8 to synthesize Prussian Blue film with the highest catalytic activity

Obviously, labile electrocatalyst (PB) has to be covered with sta-bilization layer (nickel hexacyanoferrate (NiHCF)) Both high op-erational stability and electrocatalytic activity are desirable Hence the reasonable optimization parameter is the sensitivity (S), evaluated from the slope of the calibration graph, multiplied by the time during which the modified electrode remains its current at the level>95%

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Journal of The Electrochemical Society, 164 (5) B3056-B3058 (2017) B3057

1 2 3

10 15 20

2

3

t9

-1 ⋅c

[NiHC F],nm

ol⋅cm

-2

[P

-2

Figure 1 Sensitivity multiplied by t95% in 1 mM H 2 O 2 as a function of

iron- and nickel hexacyanoferrates surface coverages; 0.0 V Ag |AgCl, 0.05 M

phosphate buffer pH 6.0 with 0.1 M KCl, upon stirring.

(t95%) from its initial value Operational stability has been investigated

under hard conditions: in 1 mM H2O2upon stirring

The 3-D plot displaying the optimization parameter as a function

of hexacyanoferrate surface coverages (Figure1), has an absolute

maximum corresponding to 2.0± 0.2 nmol cm−2 of Prussian Blue

and 2.4± 0.3 nmol cm−2of nickel hexacyanoferrate This particular

point also corresponds to the highest operational stability of the

elec-trocatalyst In hard conditions under 1 mM H2O2the electrode does

not displays any decay in current response during more than one hour

The proposed approach is also characterized by a high

reproducibil-ity: variation in both sensitivity and t95%among 10 different modified

electrodes is less than 10%

Since lactate oxidase is much less stable than glucose oxidase,

operational stability of lactate biosensors has been investigated

Re-sponse of the biosensor made on the basis of PB-NiHCF is

approxi-mately 1.5 times less compared to the lactate-sensitive electrode using

common PB as a transducer (Figure2) However, the response

cur-rent of the bilayer based biosensor is much more stable: the time of

half inactivation (≈7.5 hours) is almost twice of it for conventional

Prussian Blue based lactate biosensor (≈4.0 hours) The current-time

dependencies in Figure2seem to obey the pseudo first order

inac-tivation after approximately 3 hours The corresponding inacinac-tivation

constants, evaluated replotting Figure2in semi-logarithmic plots, in

case of PB-NiHCF bilayer for monitoring of 0.25 mM and 0.5 mM

lactate are of k in≈ 1.2 · 10−3 min−1 and k

in≈ 1.8 · 10−3 min−1, re-spectively Lactate biosensors made on the basis of conventional PB

display inactivation constants of k in≈ 4.1 · 10−3 min−1in 0.25 mM

0

-15

-30

t, h

PB-NiHCF PB

Figure 2 Operational stability of lactate biosensors made on the basis of PB

and PB-NiHCF bilayer; 0.0 V Ag |AgCl, 0.25 mM lactate in 50 mM phosphate,

pH 6.0, with 0.1 M KCl, upon stirring.

10-1 1 10

102

0 -20

-40

[Lactate], M

1⋅10 -5 M

t, s

5⋅10 -3

M 1⋅10 -3 M 5⋅10 -4

M

1⋅10 -4 M 5⋅10 -5 M

Figure 3 Calibration graphs for lactate biosensors made on the basis of

com-mon Prussian Blue (o) and PB-NiHCF bilayer ( •);0.0 V Ag|AgCl, 50 mM phosphate, pH 6.0, with 0.1 M KCl, upon stirring Inset: response of the biosensor based on PB-NiHCF bilayer to lactate.

lactate and of k in≈ 6.0 · 10−3min−1in 0.5 mM lactate Hence, the im-proved operational stability of lactate biosensors based on PB-NiHCF can be characterized in terms of≈3.5 times decreased inactivation constants

Not surprisingly, for more stable enzyme, glucose oxidase, the operational stability can also be improved using the more stable transducer The time for twofold decrease of the current response for the bilayer based biosensor (≈27.5 hours) is also twice of it for conventional Prussian Blue based glucose biosensor (≈14.0 hours) The corresponding inactivation constants for PB-NiHCF and for PB

based transducers are k in ≈ 3.7 · 10−4 min−1 and 8.1· 10−4 min−1, respectively

Such improvement of the operational stability is of particular im-portance for continuous monitoring of metabolites with wearable devices

Calibration graphs of lactate biosensors in batch mode are dis-played in Figure 3 Despite lactate biosensor made on the basis of PB-NiHCF bilayer displays lower response, for both biosensors the dynamic range is similar: from 1μM to 5 mM Hence, a slightly lower sensitivity of the biosensor based on PB-NiHCF bilayer does not affect the dynamic range, and the biosensor is suitable for similar tasks as the lactate sensitive electrode based on conventional Prussian Blue As expected, no current decay between injections of the analyte can be registered (Figure3, inset) A noise at high lactate concentra-tions is due to solution turbulence around planar sensor structure upon stirring

The dynamic ranges for Prussian Blue based and PB-NiHCF bi-layer based glucose biosensors are similarly prolonged from 1μM to

10 mM analyte concentrations

Summary

Operational stability of the oxidase-based biosensors, which is of particular importance especially for wearable devices, can be signif-icantly improved stabilizing the transducer used Prussian Blue (PB) based advanced hydrogen peroxide transducer, 1000 times more active and selective than platinum, which allows H2O2detection by reduction

in the presence of oxygen, and in contrast to Pt is suitable for analysis

of excretory liquids like sweat, is deposited onto screen-printed elec-trode structures and stabilized with nickel hexacyanoferrate (NiHCF), both in open circuit mode Operational stability of PB-NiHCF bilayer based biosensors and even apparently the most labile lactate oxidase

is significantly improved in terms of twice longer half inactivation and ≈3.5 times lower inactivation constant The dynamic range of PB-NiHCF based biosensors is similar to it for conventional PB based ones, which allows using the former for similar purposes drastically improving their performance characteristics

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B3058 Journal of The Electrochemical Society, 164 (5) B3056-B3058 (2017)

Acknowledgments

Financial support through Russian Science Foundation grant #

16-13-00010 is greatly acknowledged

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