PMC:7152911 / 89983-107911 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7152911","sourcedb":"PMC","sourceid":"7152911","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7152911","text":"3.3 Electrochemical methods for pathogen detection using electrochemical biosensors\nVarious electrochemical methods can be performed using functionalized electrodes to enable pathogen detection (Bard and Faulkner, 2000). These methods differ in electrode configuration, applied signals, measured signals, mass transport regimes, binding information provided (Thévenot et al. 2001), and target size-selectivity (Amiri et al. 2018). Electrochemical methods used for pathogen detection can be classified as potentiometric, amperometric, conductometric, impedimetric, or ion-charge/field-effect, which often signify the measured signal (Thévenot et al. 2001). The applied signals may be constant or time-varying. The result of the electrochemical method may require analysis of the output signal's transient response, steady-steady response, or a combination of both. A detailed discussion of the aforementioned electrochemical methods has been provided elsewhere (Bard and Faulkner, 2000). Here, we briefly review the most recent methods employed for pathogen detection using electrochemical biosensors.\n\n3.3.1 Potentiometry\nPotentiometric methods, also referred to as controlled-current methods, are those in which an electrical potential is measured in response to an applied current (Bard and Faulkner, 2000). The applied current is typically low amplitude. An advantage of controlled-current methods is the ability to use low-cost measurement instrumentation relative to that required for controlled-potential methods.\nHai et al. used potentiometry with a conductive polymer-based biosensor to detect human influenza A virus (H1N1) at a LOD of 0.013 HAU (Hai et al. 2017). Hernandez et al. used potentiometry with a carbon-rod modified electrode that contained reduced graphene oxide to detect S. aureus at a single CFU/mL (Hernandez et al. 2014). Boehm et al. detected E. coli via potentiometry utilizing a Pt wire electrode (Boehm et al. 2007). Further studies utilizing potentiometric sensing approaches are listed in Table 1, Table 2.\n\n3.3.2 Voltammetry\nVoltammetric methods, also referred to as controlled-potential methods, are those in which a current is measured in response to an applied electrical potential that drives redox reactions (Bard and Faulkner, 2000). The measured current is indicative of electron transfer within the sample and at the electrode surface, and thus, the concentration of the analyte. In chronoamperometry, the electrical potential at the working electrode is applied in steps, and the resulting current is measured as a function of time. The applied electrical potential can also be held constant or varied with time as the current is measured.\nAlthough various types of biosensors are compatible with voltammetry-based measurements, field-effect transistor (FET)-based biosensors often utilize amperometric-based methods for pathogen detection (Huang et al. 2011; Liu et al. 2013). FET biosensors detect pathogens via measured changes in source-drain channel conductivity that arise from the electric field of the sample environment. This is achieved by immobilizing biorecognition elements on the metal or polymer gate electrode of the device. He et al. showed that FETs based on PEDOT:PSS organic electrochemical transistor electrodes enabled the detection of E. coli in KCl solutions using Pt and Ag/AgCl gate electrodes (He et al. 2012). Wu et al. used a graphene-based FET to detect E. coli in nutrient broth diluted with phosphate buffered saline solution with amperometry using a Ag/AgCl gate electrode (Wu et al. 2016).\nFurther examples of amperometric sensing include the detection of human influenza A virus by Singh et al. using a reduced graphene oxide-based electrode and chronoamperometry using Fe(CN)6 3 - /4- at a LOD of 0.5 plaque-forming units (PFU)/mL (Singh et al. 2017b). Lee and Jun utilized wire-based electrodes for amperometric detection of E. coli and S. aureus (Lee and Jun 2016). A detailed list of studies that utilize amperometric methods for pathogen detection is provided in Table 1, Table 2\n\n3.3.2.1 Linear sweep and cyclic voltammetry\nLinear sweep voltammetry (LSV) methods are those in which a current is measured in response to an applied electrical potential that is swept at a constant rate across a range of electrical potentials (Bard and Faulkner, 2000). Cyclic voltammetry (CV) is a commonly used linear-sweep method in which the electrical potential is swept in both the forward and reverse directions in partial cycles, full cycles, or a series of cycles. CV is one of the most widely used voltammetric methods for pathogen detection.\nHong et al. used sweep voltammetry to detect norovirus in a sample solution with Fe(CN)6 3 - /4- extracted from lettuce (Hong et al. 2015). A typical CV response using Fe(CN)6 3 - /4- associated with pathogen detection is shown in Fig. 5 a for various concentrations of E. coli binding to a polymer composite electrode (Güner et al. 2017). A detailed overview of pathogen detection studies based on CV is provided in Table 1, Table 2.\nFig. 5 Typical responses associated with the common electrochemical methods used for pathogen detection. a) Cyclic voltammetry (CV) data using Fe(CN)63-/4- for varying concentrations of E. coli (Güner et al. 2017). b) Differential pulse voltammetry (DPV) data using Fe(CN)63-/4- for varying concentrations of S. aureus (Bhardwaj et al. 2017). c) Electrochemical impedance spectroscopy (EIS) in 100 mM LiClO4 solution in the form of a Nyquist plot and corresponding equivalent circuit model associated with biorecognition element immobilization and detection of S. typhimurium (Sheikhzadeh et al. 2016). d) Conductometry data for varying concentrations of B. subtilis (Yoo et al. 2017).\n\n3.3.2.2 Pulse voltammetry\nPulse voltammetry is a type of voltammetry in which the electrical potential is applied in pulses. The technique has the advantage of improved speed and sensitivity relative to traditional voltammetric techniques (Bard and Faulkner, 2000; Molina and González, 2016). In staircase voltammetry, the electrical potential is pulsed in a series of stair steps and the current is measured following each step change, which reduces the effect of capacitive charging on the current signal. Square wave voltammetry (SWV) is a type of staircase voltammetry that applies a symmetric square-wave pulse superimposed on a staircase potential waveform. The forward pulse of the waveform coincides with the staircase step. In differential pulse voltammetry (DPV), the electrical potential is scanned with a series of fixed amplitude pulses and superimposed on a changing base potential. The current is measured before the pulse application and again at the end of the pulse, which allows for the decay of the nonfaradaic current (Scott, 2016).\nFor example, Iqbal et al. used SWV with AuNP-modified carbon electrodes for detection of C. parvum in samples taken from fruit (Iqbal et al. 2015). Kitajima et al. also used SWV with Au microelectrodes to detect norovirus at a LOD of 10 PFU/mL (Kitajima et al. 2016). Cheng et al. used DPV and a nanostructured alumina electrode for detection of dengue type 2 virus with a LOD of 1 PFU/mL (Cheng et al. 2012). As shown in Fig. 5b, Bhardwaj et al. used DPV with a carbon-based electrode to detect S. aureus (Bhardwaj et al. 2017). Additional studies that utilize pulse voltammetry methods forpathogen detection are listed in Table 1, Table 2.\n\n3.3.2.3 Stripping voltammetry\nMany of the previously described voltammetric methods can be modified to include a step that pre-concentrates the target on the electrode surface. Subsequently, the pre-concentrated target is stripped from the surface by application of an electrical potential. In anodic stripping voltammetry (ASV), a negative potential is used to pre-concentrate metal ions onto the electrode surface. These ions are then stripped from the surface by applied positive potentials. Although most commonly used to detect trace amounts of metals, this method has been adapted for pathogen detection by electrocatalytically coating metallic labels on bound targets for oxidative stripping and subsequently measuring the current response (Abbaspour et al. 2015).\nChen et al. used stripping voltammetry with a polymer-CNT composite-based electrode to detect E. coli at a LOD of 13 CFU/mL (Chen et al. 2014). In that study, the biosensor was first incubated with E. coli. Silica-coated Ag nanoparticles conjugated with anti-E.coli were subsequently introduced to the system, inducing a binding reaction between the bacteria and the nanoparticles. After rinsing non-specifically bound particles, acid was introduced to dissolve Ag(s), and the resulting Ag+-rich solution was characterized using DPV. Viswanathan et al. used ASV with screen-printed composite electrodes for multiplexed detection of Campylobacter, S. typhimurium, and E. coli with a LOD of 400 cells/mL, 400 cells/mL, and 800 cells/mL, respectively (Viswanathan et al. 2012). In that study, antibody-functionalized nanocrystalline bioconjugates were first introduced to biosensor-bound bacteria, the specifically bound particles were dissolved with acid, and the ions were then stripped using a square-wave voltammetric waveform. Additional studies using stripping voltammetry for electrochemical detection of pathogens can be found in Table 1, Table 2.\n\n3.3.3 Electrochemical impedance spectroscopy\nThe aforementioned electrochemical methods involved responses based on step changes or continuous sweeps in the applied current or voltage that drove the electrode to a condition far from equilibrium. Alternatively, frequency response methods, often referred to as impedance-based or impedimetric methods, are based on frequency response analysis (i.e., the response of the system to periodic applied current or potential waveforms at either a fixed frequency or over a range of frequencies) (Bard and Faulkner, 2000). This provides several advantages, including measurement over a wide range of times and frequencies and high precision in time-averaged responses. We next discuss impedance-based electrochemical methods for detection of pathogens using electrochemical biosensors.\nIn EIS the impedance and phase angle of the system are measured as a function of the frequency of the applied electrical potential. EIS is a diverse electrochemical method, which can be done as a faradaic or non-faradaic process, and enables the study of intrinsic material properties, experiment-specific processes, or biorecognition events at the electrode surface. EIS is often performed using an applied low-amplitude sinusoidal electrical potential and a three-electrode configuration. Equivalent circuit models are commonly fit to experimental impedance and phase angle data to interpret the electrochemical process in terms of passive circuit elements, such as resistors and capacitors. For example, the electric double layer is typically modeled as a capacitive element, while the resistance to faradaic charge transfer at the electrode-electrolyte interface is represented as a resistor, often referred to as the charge transfer resistance. Additional circuit elements, such as constant-phase or Warburg elements, can also be included to represent other features of the electrochemical cell and process, such transport characteristics of the species at the electrode-electrolyte interface. The Randles model is a commonly used equivalent circuit for interpretation of biosensor EIS data. The circuit consists of an electrolyte resistance in series with a parallel combination of the double-layer capacitance with the charge transfer resistance and the Warburg impedance element (Randles, 1947). Variations of this model have been formulated for a variety of biosensing studies. For example, the equivalent circuit model and associated Nyquist plot for electrochemical detection of S. typhimurium using EIS with a poly(pyrrole-co-3-carboxyl-pyrrole) copolymer supported aptamer can be found in Fig. 5c (Sheikhzadeh et al. 2016). The equivalent circuit model consists of the solution resistance, charge transfer resistance at the copolymer-aptamer/electrolyte interface, and constant phase element for the charge capacitance at the copolymer-aptamer/electrolyte interface (Sheikhzadeh et al. 2016).\nWhile the impedance can be measured across a range of frequencies and interpreted using equivalent circuit models that describe impedance response over a wide frequency range, fixed-frequency measurements are also useful for biosensing applications. Fixed-frequency measurements are typically based on the identification of single frequencies or small frequency ranges in the impedance spectra that are most sensitive to molecular binding events. Fixed-frequency approaches have the advantage of increasing the sampling frequency of the biosensor. As a result, impedance-based electrochemical methods generate biosensor responses in terms of changes in the measured physical quantities (e.g., changes in impedance) or calculated equivalent circuit elements (e.g., double-layer capacitance or charge-transfer resistance).\nAs shown in Table 1, Table 2, EIS is one of the most commonly used methods for electrochemical detection of pathogens. For example, Zarei et al. used EIS with an Au nanoparticle-modified carbon-based electrode for detection of Shigella dysenteriae (S. dysenteriae) at a LOD of 1 CFU/mL (Zarei et al. 2018). Primiceri et al. used EIS with Au interdigitated microelectrode arrays and Fe(CN)6 3 - /4- to detect L. monocytogenes at a LOD of 5 CFU/mL (Primiceri et al. 2016). Andrade et al. used EIS with a CNT-based electrode for multiplexed detection of E. coli, B. subtilis, and Enterococcus faecalis (Andrade et al. 2015).\nRedox reactions at the electrode-electrolyte interface are typically established using a redox probe. Owing to its high reversibility, the Fe(CN)6 3 - /4- redox couple has been widely investigated as an electrochemical probe for biosensing applications and is regarded as a standard model for highly reversible electrochemical reactions (Daum and Enke, 1969). While useful electrochemical probes, redox reactions may also affect the electrode and immobilized biorecognition elements. For example, redox reactions associated with the Fe(CN)6 3 - /4- probe can cause etching of Au electrodes due to the presence of CN− ions when using the redox couple for EIS measurements (Vogt et al. 2016). This observation warrants further investigation, particularly in the context of establishing the effects on biosensor repeatability and reusability. The use of alternative redox probes or electrode materials may mitigate such effects. For example, ferrocene and ferrocenemethanol have also been used as redox probes for pathogen detection. Ruthenium(III)/ruthenium(II) (Schrattenecker et al. 2019) and immobilized quinone pairs (Piro et al. 2013) are also potentially useful alternatives.\nBiosensors that use impedance-based methods and whose impedance response can be modeled using equivalent circuit models can be used to calculate the capacitance of the electric double layer. The double-layer capacitance is recognized to be sensitive to the structure of the electrode, the characteristics and concentration of analytes at the electrode surface and in the electrolyte, and the characteristics of the electrolyte (Lisdat and Schäfer, 2008). As a capacitor, the double-layer is not only dependent on the dielectric material but also the thickness of the dielectric layer. Importantly, both characteristics could be affected by molecular binding events on an electrode. For example, when a target analyte binds to an immobilized biorecognition element, counter ions around the electrode surface are displaced, leading to a change in the capacitance (Berggren et al. 2001). The capacitance can be determined from the reactive component of the impedance or by fitting of an equivalent circuit model (Barsoukov and Macdonald, 2018).\nIdil et al. used the capacitive response of a MIP electrode for the detection of E. coli (Idil et al. 2017). Jantra et al. similarly used the capacitive response of an Au rod electrode for the detection of E. coli (Jantra et al. 2011). Luka et al. used the capacitive response of an Au interdigitated microelectrode array based on equivalent circuit analysis for the detection of C. parvum (Luka et al. 2019). See Table 1, Table 2 for a detailed list of studies that have used the capacitive response of an electrochemical biosensor for pathogen detection.\n\n3.3.4 Conductometry\nConductometry methods are those in which the conductivity of the sample solution is monitored using a low-amplitude alternating electrical potential (Dzyadevych and Jaffrezic-Renault, 2014). The principle relies on conductivity change in the sample via the production or consumption of charged species. The measurement has the advantage of not requiring a reference electrode and can be used to detect both electroactive and electroinactive analytes (Jaffrezic-Renault and Dzyadevych, 2008; Narayan, 2016). Given the method can be performed using a two-electrode configuration, conductometric biosensors can be easily miniaturized. In addition, they are less vulnerable to many types of interference due to their differential measurement mode (Jaffrezic-Renault and Dzyadevych, 2008).\nAs shown in Fig. 5d, Yoo et al. used a conductometric biosensor with CNT-based electrodes for the detection of B. subtilis (Yoo et al. 2017). Mannoor et al. used a previously described conductometric biosensor to detect S. aureus and Helicobacter pylori on tooth enamel (Mannoor et al. 2012). Shen et al. detected two strains of human influenza A virus (H1N1 and H3N2) using conductometry with a silicon nanowire array at a LOD of 29 viruses/μL (Shen et al. 2012). Additional studies that have examined the use of conductometric biosensors for pathogen detection can be found in Table 1, Table 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