Abstract
Electrochemical impedance spectroscopy (EIS) is a sensitive technique for the analysis of the interfacial properties related to biorecognition events such as reactions catalyzed by enzymes, biomolecular recognition events of specific binding proteins, lectins, receptors, nucleic acids, whole cells, antibodies or antibody-related substances, occurring at the modified surface. Many studies on impedimetric biosensors are focused on immunosensors and aptasensors. In impedimetric immunosensors, antibodies and antigens are bound each other and thus immunocomplex is formed and the electrode is coated with a blocking layer. As a result of that electron transfer resistance increases. In impedimetric aptasensors, impedance changes following the binding of target sequences, conformational changes, or DNA damages. Impedimetric biosensors allow direct detection of biomolecular recognition events without using enzyme labels. In this paper, impedimetric biosensors are reviewed and the most interesting ones are discussed.
Introduction
The pioneering study of Clark and Lyons, more than four decades ago, shed light on some analytical researches in designing of biosensors, which perform as economical and fast tools for clinical, chemical, environmental, and pharmaceutical studies. Because of its simple use and portability in relatively complex samples, biosensors offer a potential alternative to advanced bioanalytical systems (CitationJin et al. 2011).
Electrochemical impedance spectroscopy (EIS) appears to be an excellent technique for the investigation of both bulk and interfacial electrical properties of electrode systems which can be used to determine quantitative parameters of electrochemical processes. If biorecognition events occur at the modified surfaces, the interfacial properties change. Shortly, EIS provides a fingerprint of the interfacial region (CitationMaalouf et al. 2007).
Electrochemical reactions, known as electron transfers at the electrode surface, involve electrolyte resistance, adsorption of electroactive species, charge transfer at the electrode surface, and mass transfer from the bulk solution to the electrode surface. Each reaction process is represented by an electrical circuit that consists of resistance, capacitors, or constant phase elements combined in parallel or in series. The most favorite model of electrical circuit for a simple electrochemical reaction is the Randles–Ershler electrical equivalent circuit model, consisting of electrolyte resistance (Rs), charge-transfer resistance (Rct) at the electrode/electrolyte interface, double-layer capacitance (Cdl), and mass transfer resistance (Rmt), also Warburg impedance (W). The solution resistance is determined by the solution conductivity and the geometry of the reaction cell, namely the distance between the electrodes and the cross-sectional area of solution linking the electrodes. The double layer capacitance displays the electrostatic interplay between the electrode and the electrolyte and depends on the electrode area, nature, the electrolyte ionic strength, and permittivity. Together, Rct and W make up the faradaic impedance. Rct reflects the charge transfer kinetics and can be thought of as the ratio of overpotential to current in absence of mass transfer limitation. Equivalent circuit models can be partially or completely empirical, each circuit component comes from a physical process in the electrochemical cell and has a characteristic impedance behavior (CitationYuan et al. 2010).
The impedance spectrum of an electrochemical system which is a function of frequency can be displayed in Nyquist or Bode plots. Nyquist plots usually include a semicircle region lying on the axis followed by a straight line. The semicircle portion (at higher frequencies) corresponds to the electron-transfer-limited process, and the straight line (at low-frequency range) represents the diffusion-limited process. This spectrum can be used to extract the electron transfer kinetics and diffusional characteristics. In very fast electron transfer processes the impedance spectrum includes only the linear part, while very slow electron transfer processes are characterized by a large semicircular region (CitationYuan et al. 2010, CitationWang 2006). The diameter of the semicircle equals to the electron transfer resistance (CitationWang 2006). Bode plot is logarithm of the absolute value of impedance (Z) and the phase (Φ) are plotted against the logarithm of frequency (f).
EIS is a powerful tool for investigating the interfacial properties related to bio-recognition events occurring at the modified surfaces. One of the advantages of EIS is the small amplitude perturbation from steady state, which makes it a non-destructive technique. The impedance can be measured in the presence or absence of a redox couple, which is referred to faradic and non-faradic impedance measurement, respectively. The faradic biosensors detect biorecognition events which occur at the modified electrode by measuring the change in the faradaic current (interfacial electron transfer resistance) owing to steric hindrance caused by the biomolecular interaction and/or by the electrostatic repulsion between the free charges of the target molecules and the electroactive species in the supporting electrolyte. Redox probe selection depends on various parameters such as the charge, hydrophobicity/hydrophilicity, size of the redox couple, and the chemical and physical properties of the modified electrodes (CitationElshafey et al. 2013a).
The limitations of the EIS technique are the several requirements to obtain a valid impedance spectrum. Theoretically, there are three basic requirements for AC impedance measurements: linearity, stability, and causality. The accuracy of EIS measurement depends not only on the technical precision of the instrumentation but also on the operating procedures (CitationYuan et al. 2010).
Biosensors based on impedance
Biosensors are designed for monitoring a biological reaction at the surface of transducers (CitationHelali et al. 2006). A variety of biomolecules such as enzymes, antibodies, cells, and microorganisms are the basic detection elements. For the development of an electrochemical biosensor, the key requirement is reproducibly immobilizing these biomolecules on to the sensor surface with keeping their biological activity (CitationRezaei et al. 2014). According to literature, various strategies have been used to design impedimetric biosensors. Among these strategies are formation of surface functional groups (carboxyl, amino, etc.) through various chemistries such as silane on glass or indium tin oxide, and alkanethiol monolayers on Au to covalently link biomolecules to surfaces; the physical entrapment of biomolecules by various electrochemically formed polymers (i.e., polypyrrole and polyaniline) or gel coatings; immobilizing biomolecules within Langmuir–Blodgett (LB) films based on amphiphilic polyelectrolytes; and the layer-by-layer assembly of alternately charged polyions.
Nanostructured materials, which are very attractive owing to their unique optical, electrical, catalytical, and magnetic properties, have been used in the field of biosensors and nanoelectronic devices.
Antibody-antigen based impedimetric immunosensors
Impedimetric immunosensor is a sensitive technique for simultaneous, label-free detection of antigen–antibody binding. In impedimetric immunosensors antibodies are immobilized on the electrodes, optical fiber, or semiconductor chips, and they have attracted great interest in recent years because of their promising applications in various areas. Antibodies and antigens are bound to each other and thus immunocomplex is formed and the electrode is coated with a blocking layer. As a result of that, electron transfer changes. After antigens binding to the antibodies, the access of the redox probes is hindered to a higher degree than in the absence of antigens. Since the Faradic reaction of a redox couple hinders increasingly, the electron transfer resistance will increase and the capacitance will decrease (CitationHou et al. 2013).
The most important step in the preparation of impedimetric immunosensors is immobilization of biomolecules on the electrode surface, because it is essential to generate stable, reproducible, and selective biosensors. For example, antibodies are physically adsorbed on the gold surface; but the adsorption of antibodies directly onto the bulk metal surface leads to the denaturation and the reduction of their bioaffinity. When antibodies are adsorbed on the surface of noble metal nanoparticles can retain their activity due to the biocompatibility of these nanoparticles mainly AuNPs (CitationChullasat et al. 2011). summarizes the impedimetric immunosensors in literature.
Table I. Impedimetric immunosensors.
Antibody-binding proteins such as protein A and protein G are generally used to immobilize oriented antibodies. CitationElshafey et al. (2013a) developed an electrochemical impedance immunosensor based on the detection of cancer marker epidermal growth factor receptor (EGFR) in brain plasma. Anti EGFR antibodies bind to protein G modified electrode via their nonantigenic Fc regions.
CitationCanbaz et al. (2014) quantified HER-3 for the first time by using anti-HER-3 antibody as biorecognition element. Self-assembly of hexandithiol on a gold electrode was successfully performed and then gold nanoparticles immobilized on SAMs to enhance the surface area. Cysteamine monolayers were self assembled on the gold nanoparticles. After performing SAMs, glutaraldehyde was used as crosslinking agent to anti-HER-3 immobilization. By using BSA, active ends of the electrode surface are blocked. Finally, artificial serum samples were spiked with HER-3 and detected by the biosensor. They used the single impedance technique, which is firstly used to characterize the binding between HER-3 and anti-HER-3.
CitationHou et al. (2014) constructed a sandwich immunosensor for PSA detection. The signal was amplified based on the Ab2–AuPd–DNA toward the catalytic precipitation of 4-choloro-1-naphthol (4-CN). DNAzyme catalyzed the oxidation of 4-CN, while AuPd hybrid nanostructures not only provided a large surface coverage for immobilization of biomolecules but also promoted 4-CN oxidation to some extent. The produced insoluble benzo-4-chlorohexadienone via 4-CN was coated on the electrode surface, and hindered the electron transfer between the solution and the electrode, thus increasing the Faradaic impedance of the base electrode.
CitationXi et al. (2011) developed a label free electrochemical impedimetric biosensor based on lectin–bacteria interaction. S. cerevisiae was captured by concanavalin A (Con A) interface through the interaction of Con A with the glycosyl complexes on cellular surface. In the presence of mannose (Man) on the electrode surface or in the reaction solution, the Rct was decreased. The resulting electrode also showed a major decrease of the Rct, indicating the decreased amount of bound S. cerevisiae and efficient competition between Man and S. cerevisiae.
Aptamer-based impedimetric biosensors
Aptamers are artificial single-stranded DNA or RNA oligonucleotides (typically smaller than 100 mer). They are selected from large randomized oligonucleotide libraries by SELEX (systematic evolution of ligands by exponential enrichment). Different types of target molecules including proteins, small molecules, cells, viruses and bacteria, and amino acids can be bound specifically to aptamers with high affinity. Aptamers have presented some superior features such as high specificity of binding affinity, better stabilization, and longer shelf life when compared to antibodies (CitationErdem et al. 2014).
Electrochemical nucleic acid sensors (genosensors) provide sensitive and inexpensive nucleic acid detection in complex samples, and they require a reduced number of PCR-based amplification steps without the need for target purification (Regan et al. 2014).
In impedimetric techniques, changes in current, resistance or impedance following the binding of target sequences (hybridization), conformational changes or DNA damages can be monitored. After target binding a measurable change occurs with these modes (1) direct detection of hybridization (label-free), (2) labeling of the target nucleic acid sequences with redox active substances/nanoparticles or (3) signal probes (indirect labels) that intercalate within the stacked base pairs, electrostatically bind to the phosphate backbone or sit within the grooves of the double helix (Regan et al. 2014). summarizes the impedimetric aptamer-based biosensors in literature.
Table II. The impedimetric antibody-antigen biosensors.
Various materials such as gold nanoparticles, quantum dots, carbon nanotubes (CitationBonanni and Del Valle 2010), ZnO (CitationYumak et al. 2011), FePt/ZnS nanocore–Shell (CitationChang and Wu 2010), a mercaptoacetic acid-modified cadmium sulfide (CitationSun et al. 2007) and carbon-nanotubes/nano zirconium dioxide/chitosan (CitationYang et al. 2007), graphene oxide/gold nanoplatform (CitationGupta et al. 2013) have demonstrated that they amplify the changes in charge transfer resistance (Rct) and increase the sensitivity of DNA hybridization detection. CitationZhang et al. (2013b) used an adjunct probe for signal amplification. An adjunct probe, thiol-modified DNA sequence with 14 bases, functioned as a fixer to immobilize the dissociative element of reporter probe to form loop structure. It blocked charge transfer and amplified EIS signal. An increase of Rct in the presence of the adjunct probe was more than ten times that of Rct without adjunct probe. CitationBonanni et al. (2009) used streptavidin modified gold nanoparticles for signal amplification of impedimetric detection of DNA hybridization. It permitted rapid formation of an easily detected conjugate with biotinylated DNA through a streptavidin–biotin interaction, thus avoiding the need of synthesizing DNA modified with nanoparticles, which is a more time consuming procedure. Due to signal amplification it was possible to increase the sensitivity of the method, obtaining a comparable signal with a DNA amount 40 times lower.
The charge transfer resistance (Rct) of the electrode increased with the concentration of the target DNA hybridized with the target ss-DNA (CitationGupta et al. 2013, CitationZhang 2013). The single-base mismatched DNA sequence and double-base mismatched DNA sequence were recognized via comparing the increase of their Rct values. The results demonstrated that this DNA biosensor displayed high selectivity for the hybridization detection (CitationZhang 2013).
Thrombin was selected as target molecules for several studies in literature, because it is a major stimulus of both procoagulant and anticoagulant reactions, and thus is a key element in various pathogenesis, including leukemia, arterial thrombosis, and liver disease (CitationXu et al. 2013a). The most extensively investigated prototype thrombin-binding aptamer (TBA) is a 15-mer single-stranded DNA. After binding to thrombin, TBA forms an intermolecular quadruplex structure and restricts the activity of thrombin. The assembly of the TBA monolayer film onto the electrode surface led to a further increase in the Rct value, owing to the abundance of negative charges on TBA sugar-phosphate backbone. After incubation in thrombin, the formation of TBA–thrombin complex on the electrode surface contributed to a significant increase in the Rct value. Also, TBA–thrombin complex insulates the electron transfer between the electrode surface and electrode solution (CitationZhang et al. 2009).
Another strategy for DNA detection involves a three-component “sandwich” assay, in which the redox label is attached to a synthetic sequence specifically designed to bind an overhang portion of the probe and target DNA. These strategies need an extra chemical labeling step either in the target DNA or in the synthetic oligonucleotide which makes the process more expensive and effortful (CitationDrummond et al. 2003).
Cell-based impedimetric biosensors
In cell-based biosensors, bacterial or prokaryotic cells have been used for detection systems. Higher eukaryotic and mammalian cells are higher detection systems. Using cell for biorecognition events have advantages. They are capable of external stimuli in situ analysis, most tissue types of cell lines and a wide range of growth media are commercially available and they provide more comprehensive and complex functional information than nucleic acid and immunochemical methods (CitationBanerjee and Bhunia 2009).
Biological cells have very different electrical properties because of the cell membranes which consist of a lipid bilayer containing many proteins, where the lipid molecules are oriented with their polar groups facing outward into the aqueous environment, and their hydrophobic hydrocarbon chains pointing inward to form the membrane interior. In the inside of a cell is present membrane covered particulates, such as mitochondria, vacuoles and a nucleus, and many dissolved charged molecules. While the cell membrane is highly insulating, the interior of the cell is highly conductive. The conductivity of the cell membrane is around 10− 7 S/m, whereas the conductivity of the interior of a cell can be as high as 1 S/m (CitationPethig and Kell 1997, CitationYang and Bashir 2008).
Bacterial biosensors coupled to impedimetric detection can be classified into two types, depending on the location of the bacterial cells in the experimental set up. One type deals with measuring the impedance change caused by the interaction between the analyte and bacteria-modified electrodes. Another type deals with measuring metabolites produced by bacterial cells as a result of growth in the presence of the analyte. summarizes the impedimetric biosensors based on cells in literature.
Table III. The impedimetric biosensors based on cells.
CitationQi et al. (2013b) constructed a biosensor, in which bacteria mediated bioimprinted films were used for selective bacterial detection. Chitosan (CS) doped with reduced graphene sheets (RGSs) was electrodeposited on an indium tin oxide electrode, and the resulting RGSs–CS hybrid film served as a platform for bacterial attachment. After depositing RGSs–CS nanocomposite film onto the ITO electrode, the Rct decreased when compared with the result obtained with bare ITO electrode. As a result of graphene facilitating the charge transfer process of [Fe(CN)6]4−/3−. A much larger resistance was observed when sulfate reducing bacteria (SRB) attached onto the conductive films—because the bacteria hindered the charge transfer process. After the nonconductive CS film was formed to embed the bacteria, the Rct increased again. Subsequently, fluorine silane coupling agent was coated on the functionalized ITO electrode and the SRB were washed away by acetone to leave bioimprinted cavities. Consequently, the charge transfer resistance decreased sharply.
Enzyme-based impedimetric biosensors
Effective immobilization of enzyme onto electrode surface is one of the key steps in the fabrication of biosensors. Various immobilization strategies such as physical adsorption, covalent attachment, entrapment, cross-linking, or affinity have been used. Each immobilization method presents advantages and disadvantages. The choice of the most appropriate technique also depends on the enzyme nature, the transducer, and the associated detection mode. The best method of enzyme immobilization is related to biosensor application which requires maximum sensitivity or stability. If immobilization method causes enzyme denaturation or conformational change or if the enzyme on its active site modifies, sensitivity decreases. Enzyme denaturation and blocking of active sites cause loss of activity. The solution of this drawback is using spacer arm between the enzyme and the support under covalent binding. Techniques based on affinity interactions between enzymes and (strept)avidin molecules, lectins, or sugars allow to immobilize enzymes in an ordered and site-specific manner, thus developing efficient biosensors. Likewise, self-assembled monolayer-based immobilization reduces the number of random orientations, generates uniform, reproducible and stable structures with high coverage (CitationSassolas et al. 2011).
summarizes the impedimetric biosensors based on enzymes and proteins in literature.
Table IV. The impedimetric biosensors based on enzymes and proteins.
CitationOliveira et al. (2011a) constructed a biosensor for bacterial lipopolysaccharide determination. The deposition of poly(vinyl chloride-vinyl acetate maleic acid) (PVM) on the electrode surface formed a film with a large surface area for the assembly of cysteine-coated gold nanoparticles (AuNpCys) and further immobilization of CramoLL lectin. As a result of the AuNpCys inorganic–organic composite containing an amine group with a positive charge was adsorbed on a negatively-charged PVM-modified gold electrode. Finally, negatively charged CramoLL was immobilized on the AuNpCys–PVM composite film based on an electrostatic interaction between oppositely charged species.
CitationCortina et al. (2006) developed a urea impedimetric biosensor using Röhm Pharma Eudragit S-100 ehteric polymer, which is a copolymer of methyl methacrylate and methacrylic acid that undergo a breakdown process at pH values higher than 7. In this enzymatic biosensor, urea hydrolysis by urease, which causes an increase of pH, triggers the degradation of polymer and generates an increase in capacitance, which is followed by EIS.
Conclusion
According to IUPAC, biosensor is defined as a self-contained integrated device which is capable of providing specific quantitative or semi-quantitative analytical information using a biological recognition element (biochemical receptor) which is in direct spatial contact with a transducer element. A biosensor should be clearly distinguished from a bioanalytical system, which requires additional processing steps, such as reagent addition. Furthermore, a biosensor should be distinguished from a bioprobe which is either disposable after one measurement, i.e., single use, or unable to continuously monitor the analyte concentration. Impedimetric biosensors have been designed by immobilizing bioreceptors such as antibodies, nucleic acids, enzymes, lectins, cells, and bacteria at the surface of the electrode. After binding target molecule to the electrode surface; a shift in impedance, a change in capacitance or admittance at the bulk of the electrode interface owing to the insulating properties are observed. The most important step in developing biosensors is to immobilize bioreceptors on electrode surface appropriately. In literature; covalent and affinity immobilization, physical adsorption, entrapping bioreceptors in films or gels, layer-by-layer deposition, cross-linking are used for the immobilization of receptors. Nanomaterials, thanks to their unique physical and chemical properties have recently become an interest for the design of electrochemical impedimetric biosensors. Nanomaterials, that are formed from metals, carbon, or polymeric species, exhibit high sensitivity, stability, and conductivity. Electrochemical impedance spectroscopy has been widely used by many research groups to detect DNA hybridization, antibody-antigen reactions, and enzyme reactions. It is a quite sensitive label free electrochemical technique for monitoring biorecognition events at the electrode surface. Because of this it provides low detection limit. Determination is rapid and requires short detection time. Impedimetric biosensors are reproducible, when the biorecognition elements are immobilized on the electrode surface by using strong chemical bonds such as SAM immobilization method. Many studies on impedimetric biosensors are focused on immunosensors and aptasensors. In immunosensors, antibodies and receptors are immobilized on the electrode surface. After the formation immuno reaction between antibody and antigen or receptor and factor, a change in impedance occurs. One way to enhance the response of a label-free immunosensor is to increase the amount of the immobilized antibody on the electrode surface, and another way is to immobilize antibody on an electrode surface incorporated with gold or silver nanoparticles, carbon nanotubes, and polymers such as chitosan and polyaniline. In impedimetric aptasensors, hybridization between probe and target DNA, conformation changes, or DNA damages lead to change in the impedance. High specificity of binding affinity, better stability, and larger shelf life are advantages of aptamer-based biosensors. Cell-based impedimetric biosensors are useful in external in situ analysis. Bacterial, procaryotic, and mammalian cells have been used to monitor the amount and activity of microorganisms. Few studies on enzyme-based impedimetric biosensors have been reported. These biosensors act based on detection of substrate or product of an enzyme reaction.
Declaration of interest
The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
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