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Electrochemical detection of serotonin: A new approach
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Review
Electrochemical detection of serotonin: A new approach ⁎
Kamyar Khoshnevisana,b, , Elham Honarvarfardc, Farzad Torabid,e, Hassan Malekif, ⁎ Hadi Baharifarg, Farnoush Faridbodf, Bagher Larijanib, Mohammad Reza Khorramizadeha,b, a
Biosensor Research Center, Endocrinology and Metabolism Molecular-Cellular Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran Endocrinology and Metabolism Research Center, Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran Department of Chemistry and Biomolecular Science, Clarkson University, Potsdam, NY 13699-5810, USA d School of Chemistry, College of Science, University of Tehran, Tehran, Iran e Center of Excellence in Electrochemistry, School of Chemistry, College of Science, University of Tehran, Tehran, Iran f Department of Medical Nanotechnology, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran g Department of Medical Nanotechnology, Applied Biophotonics Research Center, Science and Research Branch, Islamic Azad University, Tehran, Iran b c
A R T I C LE I N FO
A B S T R A C T
Keywords: Serotonin Electrochemical sensing Biomarker Conductive polymers Glassy carbon electrode Polymer modification
Serotonin (5-hydroxytryptamine, 5-HT) is an important neurotransmitter which plays a significant role in various functions in the body, such as appetite, emotions, and autonomic functions. It is well known that biomarker 5-HT levels can be correlated to several diseases and disorders such as depression, anxiety, irritable bowel, and sleep trouble. Among various methods for detecting the 5-HT biomarker, electrochemical techniques have attracted great interest due to their low cost and ease of operation. However, sensitive and precise electrochemical detection of 5-HT levels is not possible using bare electrodes, thus requiring electrode modification. The present review aims to describe the different electroanalytical methods for 5-HT detection using various surface-modified electrodes such as glassy carbon, carbon fiber, diamond, graphite, and metal electrodes modified with conductive polymers. Perspectives and the modification of electrode surface using applied polymers for 5-HT detection have also been presented.
1. Introduction In recent years, various biomarkers have been associated with different diseases, and the evaluation of these biomarkers has been considered to assess the health status and steps of diseases [1,2]. Neurotransmitters, specifically serotonin (5-HT), plays a key role as a biomarker [3–6] in several diseases, including depression and irritable bowel syndrome [7–10]. Moreover, 5-HT levels have been associated with hypertension neuropsychiatric disorders [11,12], neurodegenerative diseases [13,14], vascular complications in metabolic disorder [15,16], and diabetes mellitus [16–19]. Furthermore, 5-HT levels have been observed in a variety of diseases such as carcinoid tumors, depressive disorders, and diabetes. In these cases, 5-HT levels were found to be at around 300 nM and 3 nM in whole blood and cerebrospinal fluid (CSF), respectively, in patients with depressive disorder [20,21]. Lower 5-HT levels were also observed (about 5–10 nM) for type 2 diabetes [17]. In urine samples of patients with carcinoid tumors, 5-HT levels were found to be about 280 µM/24 h [22]. Normal 5-HT levels have been found to be at around 270 nM to 1490 nM in serum samples
[23], around 300–1650 nM in urine, and < 0.0568 nM in CSF [24–26]. Thus, 5-HT determination in biological fluids has attracted considerable attention based on the demand for medical diagnostic methods [27–29]. Different approaches are available for determining 5-HT levels, including HPLC-ECD and ELISA. Despite the advantages of these methods, the necessity of having simple, inexpensive, and quick approaches remains [30–32]. Electrochemical sensing strategy methods have attracted more attention for their simplicity, high sensitivity, selectivity, and low-cost detection of biomolecular analytes [33,34]. On the other hand, bare electrodes show inadequate sensitivity for the detection of 5HT due to electrochemical fouling, low concentration of 5-HT in biological samples, and the presence of interfering molecules such as dopamine (DA) and ascorbic acid [35]. One proposed strategy for overcoming these concerns is to modify the surface of the electrode to enhance its sensitivity and selectivity [36]. In the past few years, much research has been done using different electrode modifiers including polymers [37–40], carbon nanotubes [27,41,42], nanoparticles [35,43–46], and inorganic and organic
⁎ Corresponding authors at: Biosensor Research Center, Endocrinology and Metabolism Molecular-Cellular Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran. E-mail addresses: [email protected] (K. Khoshnevisan), [email protected] (M.R. Khorramizadeh).
https://doi.org/10.1016/j.cca.2019.10.028 Received 31 July 2019; Received in revised form 22 October 2019; Accepted 22 October 2019 0009-8981/ © 2019 Elsevier B.V. All rights reserved.
Please cite this article as: Kamyar Khoshnevisan, et al., Clinica Chimica Acta, https://doi.org/10.1016/j.cca.2019.10.028
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in the presence of interferences such as AA. The developed DTDB/GCE demonstrated the effective elimination of interference from AA up to a 100-fold concentration of AA. The simultaneous detection of norepinephrine (NEP) and 5-HT cannot be performed utilizing a bare GCE due to the overlapping oxidation potential and electrode fouling. Thus, as a solution for tackling this problem, a film of 3-amino-5-mercapto-1,2,4-triazole (AMTa) was employed for surface modification of a GCE. The resulting electrode, named p-AMTa modified GCE, was fabricated through the electropolymerization of AMTa on the electrode by applying potential from −0.2 V to +1.70 V at a scan rate of 50 mV s−1. Simultaneous detection of NEP and 5-HT was successfully achieved using this electrode with a potential difference of 150 mV between NEP and 5-HT [51]. Polyazines are a group of electroactive polymers with excellent electron mediating and electrocatalytic properties having potential uses in a broadening range of fields such as electrochromic displays, electrocatalysis, and microelectronic devices. Selvaraju et al. modified a GCE with poly(phenosafranine) (PPS) through the oxidation of phenonsafranine, which can be transformed into an electropolymerized film. The PPS/GC electrode demonstrated sharp voltammetric peaks at −0.05, 0.15, and 0.28 mV associated with the oxidation of AA, DA, and 5-HT, respectively [72]. Diamond electrodes demonstrate unique features compared with GCEs, including extreme electrochemical stability, wide electrochemical potentials, low voltammetric background current, and high resistance to deactivation through fouling, which makes it an excellent candidate for utilization in electrochemical sensors. A polycrystalline, boron-doped diamond thin-film electrode was fabricated to detect and study the electrochemistry of 5-HT and histamine. The results obtained from the boron-doped diamond thin-film electrodes showed highly reproducible and well-defined cyclic voltammograms compared to GCE [73,74]. Although polymer modification of the surface of electrodes provides powerful routes for the sensitive detection of 5-HT, other approaches, such as modification of electrode surfaces with bioactive species like amino acids and DNA, have opened a new avenue for designing and developing biosensing platforms. Wang et al. demonstrated a modified GCE with 5-hydroxytryptophan (5-HTP) having vigorous catalytic activity toward the oxidation of 5-HT and DA as well as two sharp voltammetric peaks for DA and 5-HT which can be utilized to determine DA and 5-HT simultaneously [75]. In another study, a simple yet highly sensitive and selective calixarene-based sensor was developed for 5-HT determination. The proposed modified electrode showed enhanced analytical presentation in the catalytic oxidation of 5-HT compared with bare GCE. Owing to the difference in potentials, this electrode can be applied as an outstanding discriminative device for 5-HT determination in the presence of DA, epinephrine (EP), AA, and folic acid as interferences [52]. Wang et al. integrated an electrochemical sensor for the detection of 5-HT by utilizing a pretreated GCE as an electron transfer enhancer coated with C-undecyl-calix resorcinarene film as a molecular receptor. A potential of +1.75 V (vs. SCE) was applied for 300 s followed by CV with a potential scan window of between 0.30 V and 1.25 V at a scan rate of 50 mVs−1. Another system for the simultaneous detection of 5HT, DA, and AA based on novel modified GCEs with the carbon-spheres (CS) system has been reported. The modified CS/GCE electrode was prepared by casting the homogenous suspension of CS in N,N-dimethylfromamide (DMF) onto the GCE surface [76]. Selvarajan et al. fabricated a novel nanocomposite comprising silver, polypyrrole, and copper oxide (Ag/PPy/Cu2O) by sonochemical and oxidative polymerization [77]. For this purpose, AgNPs-decorated Cu2O was covered by a polypyrrole (PPy) layer, and the obtained composite was dropcast on the GCE surface. The proposed system with the mentioned results represented high electrocatalytic activity, reasonable repeatability, stability, quick response, and good selectivity against potentially interfering types for 5-HT determination. The
compounds [47–49] to improve the detection of 5-HT [50–53]. Among the different electrode modifiers, polymers are widely employed, because they provide more active sites than covalently modified electrodes and excellent stability. There is a considerable amount of literature on the development of polymer-modified electrodes for 5-HT detection [54,55]. Surface modification of the above-mentioned electrodes demonstrates great enhancement in sensitivity and precision of 5-HT detection, resulting in the development of electrochemical sensors with a detection limit as low as a picomolar (pM). For example, an electropolymerized film of 3-amino-5-mercapto-1,2,4-triazole modified glassy carbon (p-AMTa) electrode was employed to detect 5-HT with a limit of detection (LOD) of 13.2 pM in the presence of norepinephrine (NEP) using differential pulse voltammetry [51]. In another study, a polymelamine-modified edge plane pyrolytic graphite sensor (EPPGE) was fabricated for the detection of 5-HT in human serum and urine samples [56]. Detection limits of 492 nM and 30 nM were found for unmodified and polymer-modified electrodes, respectively, which demonstrated enhanced sensitivity using the modified electrode [51,57–59]. The polymer-modified electrodes demonstrated high stability and great electron-mediating activity towards 5-HT, DA, and ascorbic acid (AA) [57,59–62] as well as satisfactory results for analyzing real samples in the presence of interfering molecules. The selection of appropriate polymers and methods for enhancing the electrode surface is a critical subject for the success of the modified electrode sensitive to 5-HT [59]. This paper describes various types of polymers and their modification approaches on different electrodes. Furthermore, recently developed polymer-modified electrodes for use in electrochemical approaches of 5-HT determination that can be installed for effective future clinical diagnoses are discussed. 2. Polymer modification based on glassy carbon electrode Glassy carbon electrodes (GCEs) have been widely employed for electrochemical sensing because of their remarkable physical and chemical features [63]. GCEs display a slightly low oxidation rate and an excellent chemical inertness, which makes them appropriate passive electrodes [64]. For these reasons, they have been modified with various polymers for electrochemical determination of neurotransmitters like 5-HT [65,66] and DA [67,68]. Filik et al. introduced a poly(safranine O) modified GCE as an electrochemical sensor for the detection of 5-HT in human serum. The GCE was modified by an electrooxidative polymerization of safranine O with applying potential from −0.8 to 1.2 V vs. Ag/AgCl at a scan rate of 50 mV (15 cycles). The simultaneous detection of 5-HT, AA, and DA was successfully achieved because of the relatively low current and different potentials in the electrochemical responses of AA and DA [69]. In another study, molecularly imprinted polymers (MIPs) were integrated into an impedimetric sensor using UV irradiation for the electronic detection of 5-HT in human blood plasma (Fig. 1) [70]. The results demonstrated that two functional monomers, methacrylic acid and acrylamide, are the key factors to achieving high selectivity towards 5-HT. The synthesized MIPs successfully allowed differentiating between 5-HT, its oxidized forms, and its metabolite 5-HIAA. A capacitive effect at the MIP NPs/plasma interface led to the impedimetric response related to 5-HT binding to MIP-coated sensor electrodes. This electrochemical sensor can provide a highly selective, rapid, and costeffective alternative to chromatographic techniques. Gong et al. employed a synthetic lipid of 5,5-ditetradecyl-2-(2-trimethylammonioethyl)-1,3-dioxane bromide (DTDB) self-assembled bilayer lipid membrane (BLM) onto the surface of a GCE for electrochemical detection of 5-HT [71]. The DTDB/GCE electrode was prepared by adding a DTDB/chloroform solution onto the GCE disk surface followed by immersing the electrode into a phosphate buffered solution (pH 6.0). The modified electrode showed a significant improvement in the electrochemical response of 5-HT with a decrease in overpotential of about 30 mV, which resulted in the detection of 5-HT 2
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Fig. 1. Schematic layout of the impedimetric flow cell for plasma measurements with an active channel (MIP) and a reference channel (NIP). Reproduced with permission from reference [70].
Fig. 2. Conceptual design of a nanocomposite (Ag/PPy/Cu2O) applied for 5-HT determination on GCE surface. Reproduced with permission from reference [77].
HT. The proposed system displayed a high recovery of 5‐HT directly from urine and blood serum samples. Table 1 illustrates the comparison between different polymer modification approaches on GCE and analytical methods which are exploited for the electrochemical sensing of the biomarker 5-HT with a demonstration of their limit of detection, linear range, and possible interferences. The outcomes of these studies verify the remarkable improvement of 5-HT determination with a suitable detection limit as low as a nanomolar through a synthetic polymer/MIP modifier on a GCE to attain the beneficial synergistic effects.
obtained system also provided a possible practical range of the nanocomposite material for the detection of different electroactive analytes (Fig. 2). In another study, GCEs were modified with multiwalled carbon nanotube (MWCNT) and chitosan (Cs) composite to selectively determine levodopa and 5-HT [78]. The as-prepared electrode was effectively applied for the determination of these analytes in human blood serum and urine with sensible results without the essentials of sample preparation. In a similar study, the detection of 5-HT at biological pH was carried out using a highly sensitive electrochemical sensor [79]. The fabricated sensor including MWCNT‐Cs nanocomposite (Fig. 3) on a GCE surface was applied for the selective detection of 53
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Fig. 3. SEM images of MWCNT‐chitosan nanocomposite film. Reproduced with permission from reference [79]. Table 1 Polymer modification based on the glassy carbon electrode. Modifier/electrode substrate
Method
LOD (nm)
Linear range (µM)
Samples
Interference
Refs.
AMTA modified GCE Poly safranine O /GCE MIP-based synthetic receptors synthetic receptors DTDB self-assembled BLM/ GCE poly(phenosafranine)/ GCE boron-doped diamond thin-film electrode 5-HTP, GCE CALOL film/GCE carbon spheres/GCE Ag/PPy/Cu2O/GCE GCE modified with CNT/ CS
CV, DPV SWV IS heat-transfer, DPV CV, DPV CV, HV CV CV, SWV, chronocoulometry DPV CV, DPV CV, CA, DPV
0.0132 5 4.3 NA 50 10.0 10 0.0017 30 700 12.4 80
0.001–50 0.3–1 NA 0.1–0.5 0.02–10 NA 0.01–100 5–35 0.01–10 40–750 0.01–250 0.5–130
human blood plasma Human blood sample Non-diluted blood plasma. PBS Whole blood PBS PBS PBS PB PBS PBS Human blood serum human serum and urine
[51] [69] [70] [80] [71] [72] [74] [75] [52] [76] [77] [78]
MWCNT- Cs/GCE
CV, DPV, EIS
50
0.05–16
in Serum and Artificial Urine Samples
NEP AA, DA NA His AA AA, DA His DA DA, EP, AA, FA DA, AA AA, UA AA, UA and various amino acids AA, DA, UA
[79]
Impedance spectroscopy (IS); hydrodynamic voltammetry (HV); cyclic voltammetry (CV); differential pulse voltammetry (DVP); square wave voltammetry (SWV); limit of detection (LOD); not available (NA); glassy carbon electrode (GCE); molecularly imprinted polymer (MIP); 5,5-ditetradecyl-2-(2-trimethylammonioethyl)1,3-dioxane bromide (DTDB); ascorbic acid (AA); uric acid (UA); dopamine (DA); epinephrine (EP); norepinephrine (NEP); histidine (His); folic acid (FA); phosphate buffer (PB); phosphate buffer saline (PBS); 3-amino-5-mercapto-1, 2, 4-triazole (AMTA); C-undecylcalix[4]resorcinarene (CALOL); uric acid (UA); multiwalled carbon nanotube (MWCNT); chitosan (Cs).
3. Polymer modification based on novel electrode
taste networks with a detection limit of 0.33 pM and a sensitivity of 19.1 mV/decade concentration (Fig. 4) [82]. A novel poly rutin (Ru)-modified paraffin-impregnated graphite electrode (WGE) was prepared using the electrochemical method to study the electrochemistry behavior of EP, 5-HT, and AA. The Ru/WGE electrode was fabricated by CV (1.40 V in 40 min) in 0.1 M PBS and 1.0 mM Ru. The Ru/WGE electrode demonstrated an excellent separation in oxidation peaks of EP, AA, and 5-HT which demonstrated that Ru is an efficient mediator for the oxidation of EP, 5-HT, and AA [83]. Adsorption and accumulation of the interfering species trigger fouling on the working electrode. Various strategies have been reported to eliminate electrode fouling, e.g., using self-cleaning heated electrodes, electrochemically activated CNTs, or developing novel electrode modifiers. Wei et al. fabricated a nonionic poly(2-amino-5-mercaptothiadiazole) film electrodeposited on a solid carbon paste electrode (CPE) by means of a potential scanning procedure for the selective
Recent progress in novel electrode technologies has shown high stability in real samples, improved status in in vivo studies, and multiple functionalities. Voltammetric sensors based on DA have been extensively used for the detection of 5-HT, but they have limited clinical applications, because the reaction surface of the electrode needs to be remade after each test. Liu et al. fabricated a 5-HT biosensor based on a Nafion membrane-coated colloidal gold screen-printed electrode (Nafion/CGSPE) to monitor 5-HT levels in depressed and anti-depressant-treated rats [81]. Taste information is transmitted through fibers to the brain, and 5HT plays an essential role in this transmission process. Chen et al. developed a 5-HT sensor based on a light-addressable potentiometric sensor (LAPS) chip to determine the 5-HT released from taste cells or
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Fig. 4. The scheme for 5-HT detection. (a) LAPS measurement system. (b) I–V curve moves toward right after applying 5-HT. (c) Taste cells and taste epithelium (d) were cultured on 5-HT sensitive LAPS chips. Bar: 10 µm. Reproduced with permission from reference [82].
employed to sense NE and 5-HT levels in rat CSF with high selectivity and sensitivity (Fig. 6). Table 2 shows the comparison between different polymer modification approaches and analytical methods that are utilized for the determination of 5-HT and demonstrates their limit of detection, linear range, and possible interferences. Polymer-modified electrodes have been used for 5-HT determination in a variety of samples, including whole blood, microbial spent medium, and zebrafish embryos.
determination of 5-HT, AA, and DA in pharmaceutical samples. The developed system exhibited high sensitivity and antifouling properties, which are related to the film electroneutrality and absence of electrostatic attraction of ionized species present in the electrolyte [84]. An electrochemical sensor based on a poly(3,4-ethylene dioxythiophene) (PEDOT)-modified platinum electrode in the presence of sodium dodecyl sulfate (SDS) for the detection of catecholamine compounds, including 5-HT, was reported. Hydrophobic adsorption of SDS on the surface of the PEDOT/Pt electrode caused repulsion toward the interfering compounds (e.g., UA, AA, and glucose) and the electrostatic attraction of catecholamine compounds [85]. Bliem et al. developed an ion-selective electrode based on a plasticized PVC membrane. To fabricate this potentiometric sensor, a cobaltabisdicarbollide anion [Co(C2B9H11)2] was embedded in a plasticized PVC as an ion-pair generator (Fig. 5), and the formation of an ion pair complex between the protonated 5-HT and a carborane anion leads to the determination of 5-HT levels [86]. To determine norepinephrine (NE) and 5-HT levels, Wang et al. fabricated a novel modified SPE containing MWNTs-ZnO/Cs composites [87]. The stability of this modified SPE can remain for at least 3 months refrigerated at 4 °C. Additionally, this system was successfully
4. Conclusions and perspectives GCE is the most applied electrode for electrochemical sensing of 5HT because of its excellent conductivity, ease of use, low cost, and high reproducibility. However, because of electro-chemical fouling, low 5HT concentrations in biological samples, and the co-existence of interfering molecules, sensitive detection of 5-HT with a bare electrode is not possible. In the past few years, modification of GCE surfaces has presented a significant enhancement in 5-HT detection. Other working electrodes such as diamond and novel ones have also been applied for the determination of neurotransmitters. In this review, different modification techniques using polymers for
Fig. 5. Chemical structure of the synthesized ion-pair complex [C10H13N2O] + [Co(C2B9H11)2]-. Non-specified vertexes in the carborane anion correspond to B-H units (A). Schematic illustration of the experimentally used sensor (B) and the experimental setup (C). Reproduced with permission from reference [86]. 5
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Fig. 6. Preparation process of the SPE: a—PVC sheets; b—silver conducting paths; c—working electrode; d—auxiliary electrode; e—reference electrode; and f—insulation layer. (B) Analysis of a 20 μL rat cerebrospinal fluid drop on the SPE surface. Reproduced with permission from reference [87]. Table 2 Polymer modification based on novel electrode. Modifier/electrode substrate
Method
LOD (nm)
Linear range (µM)
Samples
Interference
Refs.
Nafion membrane-coated colloidal gold SPE LAPS chip Ru modified WGE nonionic p-AMT / solid CPE PEDOT modified the platinum electrode ion-selective electrodes based on plasticized PVC membranes SPE modified with MWNTs-ZnO/Cs
DPV Modulated light CV, DPV CV CV, LSV, UV, EIS FIM
10.0 0.33 × 10−3 100 0.4 71 0.02
0.05–1.0 NA 0.3–9 0.02–1.56 20–100 22.5–10000
Blood taste tissue/cells PBS BRS B-R buffer NA
DA, AA and UA NA EP, AA AA, DA UA, AA, glucose Li+, Na+, K+, Trp, DA, EP
[81] [82] [83] [84] [85] [86]
CV, SWV
10
0.10–1.00
rat CSF
AA, UA, glucose, Ca2+, Mg2+, citric acid
[87]
Britton–Robinson buffer (BRS); interference method (FIM); linear sweep voltammetry (LSV); Fluorescence spectroscopy (FS); electrochemical impedance spectroscopy (EIS). poly(2-amino-5-mercapto-thiadiazole (p-AMT); ultraviolet–visible (UV); screen-printed electrode (SPE).
the detection of 5-HT have been discussed. Different interactions, including covalent bonding, hydrogen bonding, host-guest interaction, molecular recognition, and size-selective interaction, can be used to enhance the electron transfer between 5-HT and the electrode. Various modified carbon-based electrodes, including glassy carbon, carbon fiber, boron-doped diamond, graphite, and screen printed carbon electrodes, have been utilized as the working electrode for the electrochemical sensing of 5-HT. Polymers not only improve the biocompatibility and redox properties of the sensors, but also provide a protective layer that can reduce the fouling of 5-HT and increase the reproducibility of the results. Moreover, the effect of interfering analytes such as DA, AA, or uric acid (UA) can be discriminated by modifying electrode surfaces with various polymer materials. The progress in electrochemical 5-HT sensing strategies using conductive polymers has demonstrated a potential for application in commercial strategies of electrochemical sensors for the disease-related biomarker 5-HT within a reasonably short time framework. Conductive polymers are one of the main factors for the transformation of electrochemical sensors from the laboratory into real clinical requests.
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Review
Electrochemical detection of serotonin: A new approach ⁎
Kamyar Khoshnevisana,b, , Elham Honarvarfardc, Farzad Torabid,e, Hassan Malekif, ⁎ Hadi Baharifarg, Farnoush Faridbodf, Bagher Larijanib, Mohammad Reza Khorramizadeha,b, a
Biosensor Research Center, Endocrinology and Metabolism Molecular-Cellular Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran Endocrinology and Metabolism Research Center, Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran Department of Chemistry and Biomolecular Science, Clarkson University, Potsdam, NY 13699-5810, USA d School of Chemistry, College of Science, University of Tehran, Tehran, Iran e Center of Excellence in Electrochemistry, School of Chemistry, College of Science, University of Tehran, Tehran, Iran f Department of Medical Nanotechnology, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran g Department of Medical Nanotechnology, Applied Biophotonics Research Center, Science and Research Branch, Islamic Azad University, Tehran, Iran b c
A R T I C LE I N FO
A B S T R A C T
Keywords: Serotonin Electrochemical sensing Biomarker Conductive polymers Glassy carbon electrode Polymer modification
Serotonin (5-hydroxytryptamine, 5-HT) is an important neurotransmitter which plays a significant role in various functions in the body, such as appetite, emotions, and autonomic functions. It is well known that biomarker 5-HT levels can be correlated to several diseases and disorders such as depression, anxiety, irritable bowel, and sleep trouble. Among various methods for detecting the 5-HT biomarker, electrochemical techniques have attracted great interest due to their low cost and ease of operation. However, sensitive and precise electrochemical detection of 5-HT levels is not possible using bare electrodes, thus requiring electrode modification. The present review aims to describe the different electroanalytical methods for 5-HT detection using various surface-modified electrodes such as glassy carbon, carbon fiber, diamond, graphite, and metal electrodes modified with conductive polymers. Perspectives and the modification of electrode surface using applied polymers for 5-HT detection have also been presented.
1. Introduction In recent years, various biomarkers have been associated with different diseases, and the evaluation of these biomarkers has been considered to assess the health status and steps of diseases [1,2]. Neurotransmitters, specifically serotonin (5-HT), plays a key role as a biomarker [3–6] in several diseases, including depression and irritable bowel syndrome [7–10]. Moreover, 5-HT levels have been associated with hypertension neuropsychiatric disorders [11,12], neurodegenerative diseases [13,14], vascular complications in metabolic disorder [15,16], and diabetes mellitus [16–19]. Furthermore, 5-HT levels have been observed in a variety of diseases such as carcinoid tumors, depressive disorders, and diabetes. In these cases, 5-HT levels were found to be at around 300 nM and 3 nM in whole blood and cerebrospinal fluid (CSF), respectively, in patients with depressive disorder [20,21]. Lower 5-HT levels were also observed (about 5–10 nM) for type 2 diabetes [17]. In urine samples of patients with carcinoid tumors, 5-HT levels were found to be about 280 µM/24 h [22]. Normal 5-HT levels have been found to be at around 270 nM to 1490 nM in serum samples
[23], around 300–1650 nM in urine, and < 0.0568 nM in CSF [24–26]. Thus, 5-HT determination in biological fluids has attracted considerable attention based on the demand for medical diagnostic methods [27–29]. Different approaches are available for determining 5-HT levels, including HPLC-ECD and ELISA. Despite the advantages of these methods, the necessity of having simple, inexpensive, and quick approaches remains [30–32]. Electrochemical sensing strategy methods have attracted more attention for their simplicity, high sensitivity, selectivity, and low-cost detection of biomolecular analytes [33,34]. On the other hand, bare electrodes show inadequate sensitivity for the detection of 5HT due to electrochemical fouling, low concentration of 5-HT in biological samples, and the presence of interfering molecules such as dopamine (DA) and ascorbic acid [35]. One proposed strategy for overcoming these concerns is to modify the surface of the electrode to enhance its sensitivity and selectivity [36]. In the past few years, much research has been done using different electrode modifiers including polymers [37–40], carbon nanotubes [27,41,42], nanoparticles [35,43–46], and inorganic and organic
⁎ Corresponding authors at: Biosensor Research Center, Endocrinology and Metabolism Molecular-Cellular Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran. E-mail addresses: [email protected] (K. Khoshnevisan), [email protected] (M.R. Khorramizadeh).
https://doi.org/10.1016/j.cca.2019.10.028 Received 31 July 2019; Received in revised form 22 October 2019; Accepted 22 October 2019 0009-8981/ © 2019 Elsevier B.V. All rights reserved.
Please cite this article as: Kamyar Khoshnevisan, et al., Clinica Chimica Acta, https://doi.org/10.1016/j.cca.2019.10.028
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in the presence of interferences such as AA. The developed DTDB/GCE demonstrated the effective elimination of interference from AA up to a 100-fold concentration of AA. The simultaneous detection of norepinephrine (NEP) and 5-HT cannot be performed utilizing a bare GCE due to the overlapping oxidation potential and electrode fouling. Thus, as a solution for tackling this problem, a film of 3-amino-5-mercapto-1,2,4-triazole (AMTa) was employed for surface modification of a GCE. The resulting electrode, named p-AMTa modified GCE, was fabricated through the electropolymerization of AMTa on the electrode by applying potential from −0.2 V to +1.70 V at a scan rate of 50 mV s−1. Simultaneous detection of NEP and 5-HT was successfully achieved using this electrode with a potential difference of 150 mV between NEP and 5-HT [51]. Polyazines are a group of electroactive polymers with excellent electron mediating and electrocatalytic properties having potential uses in a broadening range of fields such as electrochromic displays, electrocatalysis, and microelectronic devices. Selvaraju et al. modified a GCE with poly(phenosafranine) (PPS) through the oxidation of phenonsafranine, which can be transformed into an electropolymerized film. The PPS/GC electrode demonstrated sharp voltammetric peaks at −0.05, 0.15, and 0.28 mV associated with the oxidation of AA, DA, and 5-HT, respectively [72]. Diamond electrodes demonstrate unique features compared with GCEs, including extreme electrochemical stability, wide electrochemical potentials, low voltammetric background current, and high resistance to deactivation through fouling, which makes it an excellent candidate for utilization in electrochemical sensors. A polycrystalline, boron-doped diamond thin-film electrode was fabricated to detect and study the electrochemistry of 5-HT and histamine. The results obtained from the boron-doped diamond thin-film electrodes showed highly reproducible and well-defined cyclic voltammograms compared to GCE [73,74]. Although polymer modification of the surface of electrodes provides powerful routes for the sensitive detection of 5-HT, other approaches, such as modification of electrode surfaces with bioactive species like amino acids and DNA, have opened a new avenue for designing and developing biosensing platforms. Wang et al. demonstrated a modified GCE with 5-hydroxytryptophan (5-HTP) having vigorous catalytic activity toward the oxidation of 5-HT and DA as well as two sharp voltammetric peaks for DA and 5-HT which can be utilized to determine DA and 5-HT simultaneously [75]. In another study, a simple yet highly sensitive and selective calixarene-based sensor was developed for 5-HT determination. The proposed modified electrode showed enhanced analytical presentation in the catalytic oxidation of 5-HT compared with bare GCE. Owing to the difference in potentials, this electrode can be applied as an outstanding discriminative device for 5-HT determination in the presence of DA, epinephrine (EP), AA, and folic acid as interferences [52]. Wang et al. integrated an electrochemical sensor for the detection of 5-HT by utilizing a pretreated GCE as an electron transfer enhancer coated with C-undecyl-calix resorcinarene film as a molecular receptor. A potential of +1.75 V (vs. SCE) was applied for 300 s followed by CV with a potential scan window of between 0.30 V and 1.25 V at a scan rate of 50 mVs−1. Another system for the simultaneous detection of 5HT, DA, and AA based on novel modified GCEs with the carbon-spheres (CS) system has been reported. The modified CS/GCE electrode was prepared by casting the homogenous suspension of CS in N,N-dimethylfromamide (DMF) onto the GCE surface [76]. Selvarajan et al. fabricated a novel nanocomposite comprising silver, polypyrrole, and copper oxide (Ag/PPy/Cu2O) by sonochemical and oxidative polymerization [77]. For this purpose, AgNPs-decorated Cu2O was covered by a polypyrrole (PPy) layer, and the obtained composite was dropcast on the GCE surface. The proposed system with the mentioned results represented high electrocatalytic activity, reasonable repeatability, stability, quick response, and good selectivity against potentially interfering types for 5-HT determination. The
compounds [47–49] to improve the detection of 5-HT [50–53]. Among the different electrode modifiers, polymers are widely employed, because they provide more active sites than covalently modified electrodes and excellent stability. There is a considerable amount of literature on the development of polymer-modified electrodes for 5-HT detection [54,55]. Surface modification of the above-mentioned electrodes demonstrates great enhancement in sensitivity and precision of 5-HT detection, resulting in the development of electrochemical sensors with a detection limit as low as a picomolar (pM). For example, an electropolymerized film of 3-amino-5-mercapto-1,2,4-triazole modified glassy carbon (p-AMTa) electrode was employed to detect 5-HT with a limit of detection (LOD) of 13.2 pM in the presence of norepinephrine (NEP) using differential pulse voltammetry [51]. In another study, a polymelamine-modified edge plane pyrolytic graphite sensor (EPPGE) was fabricated for the detection of 5-HT in human serum and urine samples [56]. Detection limits of 492 nM and 30 nM were found for unmodified and polymer-modified electrodes, respectively, which demonstrated enhanced sensitivity using the modified electrode [51,57–59]. The polymer-modified electrodes demonstrated high stability and great electron-mediating activity towards 5-HT, DA, and ascorbic acid (AA) [57,59–62] as well as satisfactory results for analyzing real samples in the presence of interfering molecules. The selection of appropriate polymers and methods for enhancing the electrode surface is a critical subject for the success of the modified electrode sensitive to 5-HT [59]. This paper describes various types of polymers and their modification approaches on different electrodes. Furthermore, recently developed polymer-modified electrodes for use in electrochemical approaches of 5-HT determination that can be installed for effective future clinical diagnoses are discussed. 2. Polymer modification based on glassy carbon electrode Glassy carbon electrodes (GCEs) have been widely employed for electrochemical sensing because of their remarkable physical and chemical features [63]. GCEs display a slightly low oxidation rate and an excellent chemical inertness, which makes them appropriate passive electrodes [64]. For these reasons, they have been modified with various polymers for electrochemical determination of neurotransmitters like 5-HT [65,66] and DA [67,68]. Filik et al. introduced a poly(safranine O) modified GCE as an electrochemical sensor for the detection of 5-HT in human serum. The GCE was modified by an electrooxidative polymerization of safranine O with applying potential from −0.8 to 1.2 V vs. Ag/AgCl at a scan rate of 50 mV (15 cycles). The simultaneous detection of 5-HT, AA, and DA was successfully achieved because of the relatively low current and different potentials in the electrochemical responses of AA and DA [69]. In another study, molecularly imprinted polymers (MIPs) were integrated into an impedimetric sensor using UV irradiation for the electronic detection of 5-HT in human blood plasma (Fig. 1) [70]. The results demonstrated that two functional monomers, methacrylic acid and acrylamide, are the key factors to achieving high selectivity towards 5-HT. The synthesized MIPs successfully allowed differentiating between 5-HT, its oxidized forms, and its metabolite 5-HIAA. A capacitive effect at the MIP NPs/plasma interface led to the impedimetric response related to 5-HT binding to MIP-coated sensor electrodes. This electrochemical sensor can provide a highly selective, rapid, and costeffective alternative to chromatographic techniques. Gong et al. employed a synthetic lipid of 5,5-ditetradecyl-2-(2-trimethylammonioethyl)-1,3-dioxane bromide (DTDB) self-assembled bilayer lipid membrane (BLM) onto the surface of a GCE for electrochemical detection of 5-HT [71]. The DTDB/GCE electrode was prepared by adding a DTDB/chloroform solution onto the GCE disk surface followed by immersing the electrode into a phosphate buffered solution (pH 6.0). The modified electrode showed a significant improvement in the electrochemical response of 5-HT with a decrease in overpotential of about 30 mV, which resulted in the detection of 5-HT 2
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Fig. 1. Schematic layout of the impedimetric flow cell for plasma measurements with an active channel (MIP) and a reference channel (NIP). Reproduced with permission from reference [70].
Fig. 2. Conceptual design of a nanocomposite (Ag/PPy/Cu2O) applied for 5-HT determination on GCE surface. Reproduced with permission from reference [77].
HT. The proposed system displayed a high recovery of 5‐HT directly from urine and blood serum samples. Table 1 illustrates the comparison between different polymer modification approaches on GCE and analytical methods which are exploited for the electrochemical sensing of the biomarker 5-HT with a demonstration of their limit of detection, linear range, and possible interferences. The outcomes of these studies verify the remarkable improvement of 5-HT determination with a suitable detection limit as low as a nanomolar through a synthetic polymer/MIP modifier on a GCE to attain the beneficial synergistic effects.
obtained system also provided a possible practical range of the nanocomposite material for the detection of different electroactive analytes (Fig. 2). In another study, GCEs were modified with multiwalled carbon nanotube (MWCNT) and chitosan (Cs) composite to selectively determine levodopa and 5-HT [78]. The as-prepared electrode was effectively applied for the determination of these analytes in human blood serum and urine with sensible results without the essentials of sample preparation. In a similar study, the detection of 5-HT at biological pH was carried out using a highly sensitive electrochemical sensor [79]. The fabricated sensor including MWCNT‐Cs nanocomposite (Fig. 3) on a GCE surface was applied for the selective detection of 53
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Fig. 3. SEM images of MWCNT‐chitosan nanocomposite film. Reproduced with permission from reference [79]. Table 1 Polymer modification based on the glassy carbon electrode. Modifier/electrode substrate
Method
LOD (nm)
Linear range (µM)
Samples
Interference
Refs.
AMTA modified GCE Poly safranine O /GCE MIP-based synthetic receptors synthetic receptors DTDB self-assembled BLM/ GCE poly(phenosafranine)/ GCE boron-doped diamond thin-film electrode 5-HTP, GCE CALOL film/GCE carbon spheres/GCE Ag/PPy/Cu2O/GCE GCE modified with CNT/ CS
CV, DPV SWV IS heat-transfer, DPV CV, DPV CV, HV CV CV, SWV, chronocoulometry DPV CV, DPV CV, CA, DPV
0.0132 5 4.3 NA 50 10.0 10 0.0017 30 700 12.4 80
0.001–50 0.3–1 NA 0.1–0.5 0.02–10 NA 0.01–100 5–35 0.01–10 40–750 0.01–250 0.5–130
human blood plasma Human blood sample Non-diluted blood plasma. PBS Whole blood PBS PBS PBS PB PBS PBS Human blood serum human serum and urine
[51] [69] [70] [80] [71] [72] [74] [75] [52] [76] [77] [78]
MWCNT- Cs/GCE
CV, DPV, EIS
50
0.05–16
in Serum and Artificial Urine Samples
NEP AA, DA NA His AA AA, DA His DA DA, EP, AA, FA DA, AA AA, UA AA, UA and various amino acids AA, DA, UA
[79]
Impedance spectroscopy (IS); hydrodynamic voltammetry (HV); cyclic voltammetry (CV); differential pulse voltammetry (DVP); square wave voltammetry (SWV); limit of detection (LOD); not available (NA); glassy carbon electrode (GCE); molecularly imprinted polymer (MIP); 5,5-ditetradecyl-2-(2-trimethylammonioethyl)1,3-dioxane bromide (DTDB); ascorbic acid (AA); uric acid (UA); dopamine (DA); epinephrine (EP); norepinephrine (NEP); histidine (His); folic acid (FA); phosphate buffer (PB); phosphate buffer saline (PBS); 3-amino-5-mercapto-1, 2, 4-triazole (AMTA); C-undecylcalix[4]resorcinarene (CALOL); uric acid (UA); multiwalled carbon nanotube (MWCNT); chitosan (Cs).
3. Polymer modification based on novel electrode
taste networks with a detection limit of 0.33 pM and a sensitivity of 19.1 mV/decade concentration (Fig. 4) [82]. A novel poly rutin (Ru)-modified paraffin-impregnated graphite electrode (WGE) was prepared using the electrochemical method to study the electrochemistry behavior of EP, 5-HT, and AA. The Ru/WGE electrode was fabricated by CV (1.40 V in 40 min) in 0.1 M PBS and 1.0 mM Ru. The Ru/WGE electrode demonstrated an excellent separation in oxidation peaks of EP, AA, and 5-HT which demonstrated that Ru is an efficient mediator for the oxidation of EP, 5-HT, and AA [83]. Adsorption and accumulation of the interfering species trigger fouling on the working electrode. Various strategies have been reported to eliminate electrode fouling, e.g., using self-cleaning heated electrodes, electrochemically activated CNTs, or developing novel electrode modifiers. Wei et al. fabricated a nonionic poly(2-amino-5-mercaptothiadiazole) film electrodeposited on a solid carbon paste electrode (CPE) by means of a potential scanning procedure for the selective
Recent progress in novel electrode technologies has shown high stability in real samples, improved status in in vivo studies, and multiple functionalities. Voltammetric sensors based on DA have been extensively used for the detection of 5-HT, but they have limited clinical applications, because the reaction surface of the electrode needs to be remade after each test. Liu et al. fabricated a 5-HT biosensor based on a Nafion membrane-coated colloidal gold screen-printed electrode (Nafion/CGSPE) to monitor 5-HT levels in depressed and anti-depressant-treated rats [81]. Taste information is transmitted through fibers to the brain, and 5HT plays an essential role in this transmission process. Chen et al. developed a 5-HT sensor based on a light-addressable potentiometric sensor (LAPS) chip to determine the 5-HT released from taste cells or
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Fig. 4. The scheme for 5-HT detection. (a) LAPS measurement system. (b) I–V curve moves toward right after applying 5-HT. (c) Taste cells and taste epithelium (d) were cultured on 5-HT sensitive LAPS chips. Bar: 10 µm. Reproduced with permission from reference [82].
employed to sense NE and 5-HT levels in rat CSF with high selectivity and sensitivity (Fig. 6). Table 2 shows the comparison between different polymer modification approaches and analytical methods that are utilized for the determination of 5-HT and demonstrates their limit of detection, linear range, and possible interferences. Polymer-modified electrodes have been used for 5-HT determination in a variety of samples, including whole blood, microbial spent medium, and zebrafish embryos.
determination of 5-HT, AA, and DA in pharmaceutical samples. The developed system exhibited high sensitivity and antifouling properties, which are related to the film electroneutrality and absence of electrostatic attraction of ionized species present in the electrolyte [84]. An electrochemical sensor based on a poly(3,4-ethylene dioxythiophene) (PEDOT)-modified platinum electrode in the presence of sodium dodecyl sulfate (SDS) for the detection of catecholamine compounds, including 5-HT, was reported. Hydrophobic adsorption of SDS on the surface of the PEDOT/Pt electrode caused repulsion toward the interfering compounds (e.g., UA, AA, and glucose) and the electrostatic attraction of catecholamine compounds [85]. Bliem et al. developed an ion-selective electrode based on a plasticized PVC membrane. To fabricate this potentiometric sensor, a cobaltabisdicarbollide anion [Co(C2B9H11)2] was embedded in a plasticized PVC as an ion-pair generator (Fig. 5), and the formation of an ion pair complex between the protonated 5-HT and a carborane anion leads to the determination of 5-HT levels [86]. To determine norepinephrine (NE) and 5-HT levels, Wang et al. fabricated a novel modified SPE containing MWNTs-ZnO/Cs composites [87]. The stability of this modified SPE can remain for at least 3 months refrigerated at 4 °C. Additionally, this system was successfully
4. Conclusions and perspectives GCE is the most applied electrode for electrochemical sensing of 5HT because of its excellent conductivity, ease of use, low cost, and high reproducibility. However, because of electro-chemical fouling, low 5HT concentrations in biological samples, and the co-existence of interfering molecules, sensitive detection of 5-HT with a bare electrode is not possible. In the past few years, modification of GCE surfaces has presented a significant enhancement in 5-HT detection. Other working electrodes such as diamond and novel ones have also been applied for the determination of neurotransmitters. In this review, different modification techniques using polymers for
Fig. 5. Chemical structure of the synthesized ion-pair complex [C10H13N2O] + [Co(C2B9H11)2]-. Non-specified vertexes in the carborane anion correspond to B-H units (A). Schematic illustration of the experimentally used sensor (B) and the experimental setup (C). Reproduced with permission from reference [86]. 5
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Fig. 6. Preparation process of the SPE: a—PVC sheets; b—silver conducting paths; c—working electrode; d—auxiliary electrode; e—reference electrode; and f—insulation layer. (B) Analysis of a 20 μL rat cerebrospinal fluid drop on the SPE surface. Reproduced with permission from reference [87]. Table 2 Polymer modification based on novel electrode. Modifier/electrode substrate
Method
LOD (nm)
Linear range (µM)
Samples
Interference
Refs.
Nafion membrane-coated colloidal gold SPE LAPS chip Ru modified WGE nonionic p-AMT / solid CPE PEDOT modified the platinum electrode ion-selective electrodes based on plasticized PVC membranes SPE modified with MWNTs-ZnO/Cs
DPV Modulated light CV, DPV CV CV, LSV, UV, EIS FIM
10.0 0.33 × 10−3 100 0.4 71 0.02
0.05–1.0 NA 0.3–9 0.02–1.56 20–100 22.5–10000
Blood taste tissue/cells PBS BRS B-R buffer NA
DA, AA and UA NA EP, AA AA, DA UA, AA, glucose Li+, Na+, K+, Trp, DA, EP
[81] [82] [83] [84] [85] [86]
CV, SWV
10
0.10–1.00
rat CSF
AA, UA, glucose, Ca2+, Mg2+, citric acid
[87]
Britton–Robinson buffer (BRS); interference method (FIM); linear sweep voltammetry (LSV); Fluorescence spectroscopy (FS); electrochemical impedance spectroscopy (EIS). poly(2-amino-5-mercapto-thiadiazole (p-AMT); ultraviolet–visible (UV); screen-printed electrode (SPE).
the detection of 5-HT have been discussed. Different interactions, including covalent bonding, hydrogen bonding, host-guest interaction, molecular recognition, and size-selective interaction, can be used to enhance the electron transfer between 5-HT and the electrode. Various modified carbon-based electrodes, including glassy carbon, carbon fiber, boron-doped diamond, graphite, and screen printed carbon electrodes, have been utilized as the working electrode for the electrochemical sensing of 5-HT. Polymers not only improve the biocompatibility and redox properties of the sensors, but also provide a protective layer that can reduce the fouling of 5-HT and increase the reproducibility of the results. Moreover, the effect of interfering analytes such as DA, AA, or uric acid (UA) can be discriminated by modifying electrode surfaces with various polymer materials. The progress in electrochemical 5-HT sensing strategies using conductive polymers has demonstrated a potential for application in commercial strategies of electrochemical sensors for the disease-related biomarker 5-HT within a reasonably short time framework. Conductive polymers are one of the main factors for the transformation of electrochemical sensors from the laboratory into real clinical requests.
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