Abstract
With the increasing demand for aquatic products, the requirement for the safety detection of aquatic products is also increasing. In the past decade, graphene oxide (GO) and reduced graphene oxide (r-GO) have become hot topics in many fields due to their special physical and chemical properties. With their excellent conductivity, a variety of electrochemical sensors have been developed in the fields of biology, food and chemistry. However, the unique optical properties of GO/r-GO have not yet been widely utilized. With the deepening of research, the fluorescence quenching performance of GO/r-GO has been proven to have excellent potential for building fluorescent sensors, and GO/r-GO fluorescent sensors have thus become an inevitable trend in sensor development. This review summarizes the main preparation methods of GO/r-GO and the principles of GO/r-GO fluorescent sensors comprehensively. Additionally, recent advances in utilizing GO/r-GO fluorescent sensors to detect aquatic food are discussed, including the application for the detection of harmful chemicals, microorganisms, and endogenous substances in aquatic products, such as pesticides, antibiotics and heavy metals. It is hoped that this review will help accelerate the progress in the field of analysis, and promote the establishment of an aquatic food supervision system.
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Introduction
Driven by the growth of global aquaculture, especially in Asia, world aquatic production is increasing continuously [1]. In 2020, the total global aquatic production was 214 million tons with 36 million tons of algae and 178 million tons of aquatic animals [2]. Aquatic animal products have gradually become the main source of animal protein intake for consumers [3,4,5]. However, aquatic products are vulnerable to various physical, chemical and microbiological hazards [6,7,8], such as allergens, harmful chemicals (antibiotics and pesticides), and pathogens (Salmonella spp, Escherichia coli, and Staphylococcus aureus) [9]. They are usually accumulated in humans through the food chain, affecting the safety of aquatic food products, and posing a significant threat to human health [10, 11]. Therefore, to ensure the safety of aquatic products, it is important to explore effective detection tools during processing, transportation and storage.
Traditional detection methods are generally based on chromatography, capillary electrophoresis (CE), polymerase chain reaction (PCR), enzyme-linked immunosorbent assay (ELISA), lateral flow test (LFT) and mass spectrometry (MS). For example, there have been several studies on the detection of tropomyosin based on PCR [12], LFT [13], ELISA [14] and MS [15]. However, these methods still suffer from some defects, limiting their wide applications, including complex processes, time-consuming, expensive instruments and professional skills [16]. Therefore, the development of practical, economical and efficient detection methods is significant to global food safety [17].
Graphene oxide (GO) is a common derivative of graphene, and reduced graphene oxide (r-GO) can be obtained by reducing it [18]. As a kind of novel carbon material with a single-atom-thick two-dimensional (2D) structure, GO and r-GO have the advantages of high intrinsic surface, large electron mobility, functional capability and others. Therefore, they have been widely used in the field of detection and sensing applications, including the detection of organic small molecules, inorganic ions, and biomolecules [19,20,21,22,23,24,25,26]. Because of their excellent electrical properties (high conductivity and low resistivity), they have been mainly applied in the field of electrochemical food detection sensing [27,28,29]. Although the electrochemical sensor has the advantages of good stability, repeatability and high sensitivity, drawbacks also exist. For example, the signal is easy to interfere with, the electrode surface modification is difficult, and it is not suitable for the simultaneous detection of multiple substances [30]. In recent years, food fluorescence detection sensors have been extensively developed, which take fluorescence as an output signal to reflect the content of a substance [31], and possess the advantages of high sensitivity, simple operation, and fewer samples needed for detection. Two main methods are available for improving the accuracy and sensitivity of these fluorescent sensors, including enlarging the detection signal and reducing the background signal. These can be achieved by enhancing the efficiency of fluorescent groups, prolonging the lifespan of fluorescent clusters, reducing the intensity of sample irradiation, and inhibiting the spontaneous fluorescence in the sample [32,33,34,35]. GO and r-GO have been proven to be significant fluorescence resonance energy transfer (FRET) receptors for a variety of fluorescent dyes, whose quenching effect are better than that of many other carbon materials, and can significantly reduce the detection background signal [36,37,38]. r-GO is considered a more effective quencher because of its higher visible light absorption capacity than GO [39, 40]. Therefore, as a quenching basis, the application of GO/r-GO in the field of fluorescence sensing is also very promising. Compared with other traditional detection methods (such as PCR, ELISA, MS) and new-type sensors (such as electrochemical sensors), the GO/r-GO fluorescent biosensor detection method has many advantages in terms of detection performance and application. Figure 1 summarizes the advantages of GO/r-GO fluorescent sensors.
The advantages of GO/r-GO fluorescent sensors
Currently, a number of reviews on the synthesis, characteristic, and functional modification of GO have been reported [41,42,43]. Meanwhile, several relevant reviews on the application of GO and r-GO in fluorescent sensors have been published, such as the detection of proteins, DNA, and viruses [44,45,46]. More specifically, Gao et al. [47] reviewed the construction and application of GO-DNA-based fluorescent sensors and electrochemical sensors. Similarly, Zhang et al. [48] discussed the development of graphene and GO, and the fluorescent sensors and bioanalytical systems with graphene or GO as a major component for in vivo and in vitro biological detection, suggesting that follow-up studies should address platform stability, probe release, and non-specific adsorption of other substrates, as well as the cytotoxicity of GO and r-GO to facilitate the future development of such sensors. However, despite these reviews, there is a lack of reviews on the application of GO/r-GO fluorescent sensors in food safety analysis, especially in the field of aquatic food safety.
Therefore, different from the previous reviews, this review focuses on the use of GO/r-GO fluorescent sensors in three aspects of aquatic product safety detection: hazardous chemical substances, hazardous microorganisms and their toxins, and hazardous endogenous substances, emphasizing the detection application advances of GO/r-GO fluorescent sensors. In addition, the review also compares the advantages and disadvantages of different preparation methods of GO and r-GO and points out the challenging issues and suggests future possible research directions in the GO/r-GO fluorescence sensing area. It is hoped that this review can provide a comprehensive summary of the application of GO/r-GO fluorescent sensors in aquatic product safety detection and enlighten the future development direction [49].
GO/r-GO Preparation and Principles of GO/r-GO Fluorescent Sensors
Common preparation methods of GO and r-GO include Brodie’s method, Staudenmaier’s method, Hummers’ method, chemical method, thermal method, electrochemical method, microwave-assisted method, and plasma method. Table 1 compares the advantages and disadvantages of these methods. Based on the principle of FRET between the quenched substrate and fluorescent labelling, GO/r-GO fluorescent sensors can be developed for safety detection in food and other relevant fields.
GO Preparation Methods
The polar oxygen-containing functional groups of GO are typically produced by oxidizing graphite with strong acids, such as hydroxyls (-OH), epoxides (C-O-C), ketone (C=O), and carboxylic (-COOH) [72]. Three common methods for preparing GO exist including Brodie’s method, Staudenmaier’s method and Hummers’ method, among them, Hummers’ method is the most widely used one [73].
The earliest reports of the GO preparation can be dated back to 1859 when Brodie used a fuming nitric acid system and potassium chlorate as an oxidant [50]. In order to further improve Brodie’s method, multiple additions of potassium chlorate and concentrated sulfuric acid were incorporated by Staudenmaier to improve the acidification process [53]. Different from the former, potassium permanganate was added as an oxidant to a mixture of graphite, sulfuric acid, and NaNO3 by Hummers to produce GO, which exhibited a higher degree of oxidation with a more regular structure, which was prone to swelling and layering in water [56]. Hummers’ method offered several advantages, such as the in-situ generation of nitric acid, avoiding the use of highly corrosive fuming nitric acid, replacing potassium chlorate with potassium permanganate to reduce toxic gas emissions as the release of NO2 and N2O4 gas in the reaction cannot be completely avoided, and improving the safety and environmental protection of preparation. Most of the current GO preparation experiments are improved based on Hummers’ method.
r-GO Preparation Methods
Factors such as high temperature during GO preparation often lead to the destruction of its surface structure [74]. Therefore, the reduction process should focus on reducing the oxygen content and repairing the surface structure. Currently, there are several reduction methods available for reducing GO, including chemical reduction, thermal reduction, electrochemical reduction, microwave-assisted reduction, and plasma reduction [75]. As the two most commonly used methods, chemical reduction methods are usually carried out in liquid or gas environments using strong reducing agents, such as hydrazine hydrate and hydrohalic acid [57,58,59], and thermal methods mainly include solvothermal and high-temperature annealing [60,61,62].
Besides, plasma reduction has gained increasing prominence in recent years. Various discharge methods are employed to generate plasma, including direct current discharge (DCD), glow discharge (GD), arc discharge, radiofrequency discharge (RF), and dielectric barrier discharge (DBD). Additionally, plasma can also be categorized into two types based on electron temperature: high-temperature plasma and low-temperature plasma [76]. As the fourth form of matter, plasma contains a range of active particles such as ions, electrons, free radicals and neutrals [77]. The active species in plasma can effectively sever oxygen-containing bonds present on the surface and edges of GO sheets, thus reducing the amount of oxygen functional groups in GO [78]. For example, the early report on the reduction of GO by plasma treatment was carried out by Hafiz using hydrogen as a gas medium [79]. The gas equivalent plasma reduction method commonly employs inert gases, hydrogen, nitrogen, ammonia, methane, and acetylene [76, 80, 81]. The liquid phase plasma reduction method involves the addition of alcohol, reducing sugar, and ammonia water to the solution system [82,83,84].
Principles of GO/r-GO-based Fluorescent Sensors
Many fluorescent sensors are developed based on the principle of FRET, which is a process of photoexcitation energy transfer from the donor fluorophore to the acceptor molecule [85]. The energy transfer occurs through dipole-dipole interactions between the excited state of the donor fluorophore and the ground state of the acceptor fluorophore [86].
In their study, Zhou et al. [87] highlighted the phenomenon that graphene was able to quench dye molecules adsorbed on its surface, owing to the presence of sp2 domains. This quenching property is also exhibited by GO and r-GO, making them promising candidates for developing fluorescent sensors. The use of fluorescent-labelled aptamers further enhances the functionality of GO/r-GO sensors [88]. When there is no target present, the fluorescent-labeled aptamers tend to adsorb onto the GO/r-GO surface. They are in close proximity to the GO/r-GO, allowing for efficient FRET between the aptamers (donor) and the GO/r-GO (acceptor), resulting in the transfer of energy, thus leading to either no fluorescence or weak fluorescence signals. However, due to the high specificity and affinity of aptamers, their binding with targets becomes favoured when the targets are introduced. This competition for binding sites between targets and GO/r-GO causes the aptamers to detach from the surface and form new complexes with targets. Consequently, the FRET phenomenon is abolished, allowing the fluorescence to reappear. By monitoring the change in fluorescence intensity, the concentration of the targets can be conveniently determined. It is worth noting that r-GO, compared to GO, exhibits a higher number of sp2 hybridization regions after reduction, rendering it more effective as a fluorescence quencher [89]. This property enhances the sensitivity and accuracy of r-GO-based fluorescent sensors in detecting and quantifying targets [90]. Figure 2 summarizes the detection principles of GO/r-GO fluorescent sensors.
Detection principles of GO/r-GO fluorescent sensors. A Fluorescent-labeled aptamers are added to the system containing GO/r-GO as the quenching substrate. B The aptamers are adsorbed on the GO/r-GO surface, and the fluorescence signals are quenched. C Add a solution containing the target detection substance (such as target molecule, target protein, and target heavy metal) to the system, desorption aptamer attached to the GO/r-GO surface, specific binding with the target detection object, and fluorescence signal recovery
Applications in Aquatic Food Safety Detection
As shown in Table 2, aquatic foods are prone to multiple hazards during production, packaging, transportation and storage, that can have adverse effects on human health, including chemicals (such as antibiotics, pesticides and heavy metals), microorganisms, mycotoxins, and harmful endogenous substances (for example, allergens and biotoxins) [91, 92]. In order to conduct sensitive and accurate detection of aquatic product safety, GO/r-GO fluorescent sensors have been extensively studied in detecting these hazards [93].
Hazardous Chemical Substances
Antibiotic Veterinary Drug
Antibiotics are extensively applied in the process of agriculture production and animal breeding. However, antibiotic abuse can result in unwanted residues in food, including sulfamethazine (SMZ), kanamycin, chloramphenicol (CAP) and ampicillin [118, 119]. They usually lead to serious side effects after consumption, posing a great threat to human health [96]. Sensor platforms based on GO/r-GO fluorescence quenching ability have been used to achieve qualitative and quantitative antibiotic detection.
Kou et al. [95] explored a fluorescent biosensor for detecting SMZ residues in animal-derived foods using carboxyfluorescein (FAM) labelled aptamers and GO, which achieved a low detection limit (as low as 0.35 ng/mL) and a wide dynamic range (from 2 to 100 ng/mL) under optimal conditions. Furthermore, it was effective in detecting SMZ residues in real samples. Li et al. [120] constructed a DNA probe consisting of an aptamer region for tobramycin binding and a template for amplification for detecting tobramycin, achieving a low detection limit (0.06 nM). Ye et al. [121] achieved sensitive monitoring of kanamycin by employing split aptamer (with a detection limit of 0.36 nM). Wen et al. [122] screened the truncated aptamer and built a GO-based fluorescent sensor to specifically detect nitrofurazone, achieving a detection limit of 1.13 ng/mL, which was lower than most of the other common detection methods. Liu et al. [123] realized the sensitive detection of fluoroquinolones by constructing fluorescent sensors using cadmium selenide quantum dots and GO (with a detection limit of 0.42 nM). Similarly, in order to achieve multiple antibiotics detection simultaneously (SMZ, kanamycin, and ampicillin), Youn et al. [124] applied different fluorescent modifiers for each antibiotic aptamer, namely cyanine 3 (Cy3), FAM, and cyanine 5 (Cy5), resulting in high efficiencies (94.36%, 93.94%, and 96.97% respectively). The sensor rapidly and synchronously screened multiple antibiotics with a low detection limit (1.997, 2.664, and 2.337 ng/mL respectively).
In addition to traditional fluorescent groups like FAM and rhodamine B (RhB), aggregation-induced emission (AIE) groups are also widely utilized in the detection system [125, 126]. In dilute solutions, AIE-active molecules remain unresponsive, while in aggregated states, they emit strong fluorescent signals. Zhang et al. [127] and Ning et al. [128] realized sensitive detection of CAP by introducing AIE DSA short alkyl chain derivative and hairpin structure respectively (1.26 pg/mL and 0.875 fM).
Pesticides
Pesticides are extensively used in agricultural production, resulting in the release of toxic compounds into the natural aquatic environment [129]. This contamination poses a health risk for consumers of aquatic products [130, 131]. As one of the main pest control chemicals, organophosphorus pesticides (OPs) are widely used in agriculture, having the ability to inhibit phosphatidylcholine biosynthesis in the central and peripheral nervous system [98]. Common OPs include Edifenphos (EDI), diazinon, acephate, and chlorpyrifos (CPF). Fluorescent sensors based on GO/r-GO have been developed to detect OPs residues.
Singh et al. [132] screened acephate aptamer and constructed a GO-based fluorescence sensor that exhibited excellent characteristics in real sample detection (detection limit as low as 4 ng/mL). Gaviria et al. [133] established a CPF fluorescence detection sensor on the basis of AChE (bio-mediator), GO (quenching agent) and carbon dots (fluorescent transductor). The sensor demonstrated high efficacy, achieving limits of detection as low as 0.14 ppb and 2.05 ppb for pure and commercial pesticides, respectively. The study held great significance as one of the few works that showed promising results in commercial pesticide formulation detection. Arvand et al. [134] synthesized ZnS and CdS [135] QDs capped with L-cysteine and have been widely used in various tests for their excellent luminescence properties, such as GO based fluorescent sensors for detecting EDI and diazinon with low detection limit (1.3 × 10−4 mg/L and 0.13 nM respectively), providing an effective solution for practical applications in the field of environmental and agricultural analysis. In comparison, Rong et al. [136] used the up-conversion nanoparticles (UCNPs) modified by aptamers as a fluorescence signal to detect diazinon, which improved detection accuracy (the detection limit was down to 0.023 ng/mL). The experiment also confirmed the applicability of this method not only to environmental samples but also to agricultural samples.
Paraquat (PQ) is broadly used in weeding practices and agricultural production [137, 138]. However, it poses a significant danger to human beings and animals as no effective treatment or specific antidote exists for paraquat poisoning currently. Over the last decades, numerous fatalities occurred because of ingesting PQ. Qian et al. [139] reported a 2D graphene nanosheet synthesis method by the water-soluble phosphate pillar[6] arene (PP6) in water phase exfoliated, which simultaneously combined fluorescence quenching capacity with the molecular identification property of graphene and PP6. Based on it, they reported a simple and sensitive fluorescence quenching sensor to detect PQ and showed good recovery in the actual water sample evaluation. Fipronil is a commercially developed pesticide that is widely around the world. Zhang et al. [140] achieved fipronil detection by using nitrogen-doped carbon quantum dots (NCQDs) modified aptamer (with a detection limit of 3.58 nM).
Heavy Metals
With continuous development of global industrialization, heavy metals (HMs) have become one of the main factors causing water pollution, such as cadmium (Cd2+), lead (Pb2+), chromium (Cr6+), arsenic (As3+), and mercury (Hg2+) [141,142,143,144,145,146]. HMs can accumulate via the food chain causing many health risks, and have been considered as human carcinogens even at low concentrations [102]. The detection limits for HMs in aquatic products are clearly stipulated in the food regulations of many countries.
Mo et al. [104] designed a unique fluorescence nano platform for evaluating Cd2+ sensitively using AuNCs and holey-reduced graphene oxide (HRGO) with a large specific surface area and porous structure. This study marked the first application of HRGO in the construction of fluorescent sensors, expanding its use beyond electrochemical sensors. Figure 3 describes the principle of this fluorescent biosensor for the detection of Cd2+. To further enhance Cd2+ detection accuracy, Wang et al. [147] explored a colourimetric fluorescent sensor based on AIE and integrated paper strips with a smartphone platform. Through mixing GO functionalized by blue emission ethylenediamine (EDA) with orange emission glutathione-stabilized AuNCs, the author prepared a colourimetric fluorescent sensor and also introduced Cu2+ to form fluorescent colour-changing switches. The reliability and accuracy of the detection sensor were confirmed in the detection of rice samples by a smartphone platform integrated with fluorescent paper strips, and the limit of detection was 0.1 mM eventually. This sensor not only offered high sensitivity but also demonstrated portability and convenience, providing a reliable and convenient method for evaluating aquatic food safety.
Fluorescent biosensors for the detection of Cd2+. A Preparation of HRGO: HRGO was obtained via a hydrothermal method on the basis of GO with H2O2 as an etchant and ascorbic acid as a reducing agent. B Detection principle: fluorescence was quenched by HRGO at first, and then the fluorescence was recovered due to the formation of the Cd-GSH complex [104]
Li et al. [148] and Wang et al. [149] detected Pb2+ with GO and r-GO-based fluorescence sensors, respectively. The results indicate that the latter had a lower detection line (0.17 nM), and there are two pivotal reasons for the higher sensitivity. On the one hand, in the experiment of Wang, the fluorescence recovery ability of FAM labelled probes could be enhanced effectively with the help of the construction of a strong DNA branching junction (formed by Pb2+ dependent DNAzyme and cascade CHA). On the other hand, r-GO itself shows stronger fluorescence quenching ability and aptamer adsorption capacity than GO, and can significantly reduce the background signal of detection. Ebrahim et al. [150] developed a highly selective Cr6+ sensor using a fluorescent nanocomposite based on doped polyaniline, GO QDs, and 2-acrylamido-2-methylpropanesulfonic acid capped Ag nanoparticles synthesized via in situ reaction. The detection limit of the sensor (0.0065 mg/L) was significantly lower than the WHO-permitted limit standard for Cr6+ in drinking water (50 µg/L).
Pathan et al. [151] prepared a “Turn On” As3+ biosensor with high selectivity and sensitivity by using GQDs functionalized with Fe3O4 nanoparticles (Fe-GQDs), whose detection limit (5 ppb) lower than the WHO permissible limit for As3+ in drinking water (10 µg/L) remarkably. The complexation between As3+ and Fe-GQDs induced AIE, which was not affected by any other interfering ions. The application of Fe-GQDs provided a large number of binding sites and enabled the magnetic separation of materials for reuse in continuous cycles. Sharma et al. [152] prepared a complex of GO and fluorescence dye nanoparticles with sizes ranging from 50 to 100 nm to assess the content of As3+. Meanwhile, femtosecond laser synthesis technology has also proven to have great potential in improving the sensitivity and selectivity of HMs detection sensors. Molybdenum disulfide (MoS2) and nitrogen-doped GO nanoparticles synthesized and functionalized by this technique had been used to detect several metals (Hg2+, As3+, Pb2+, and Cd2+) successfully with each detection limit lower than 15 nM [153]. Zhang et al. [154] and Li et al. [155] achieved rapid and sensitive detection of Hg2+ (the detection limit was down to 0.5 nM and 0.92 nM), with the latter having a faster response time of 5 min.
Fe3O4 magnetized GO nanoparticles and silver nanoparticle-decorated r-GO nanocomposites were also applied in the detection of Hg2+ [156, 157]. Differently, to detect Hg2+, Abdelhamid et al. [158] quenched the fluorescence of r-GO by forming a complex of Hg2+ on its surface.
Microorganisms and Toxins
Bacteria
Aquatic products are susceptible to contamination from pathogenic bacteria, which can be occurred in aquatic animals naturally, or due to mishandling during processing [9]. Common pathogenic bacteria found in aquatic products include Campylobacter jejuni (C. jejuni), Acinetobacter baumannii (A. baumannii), Staphylococcus aureus (S. aureus), Salmonella typhimurium (S. typhimurium), Helicobacter pylori (H. pylori), and Salmonella enteritidis (S. enteritidis), which would bring potential health risks to human beings [105, 159,160,161,162]. Given the higher cost of treating illnesses caused by contaminated food, it is more cost-effective to develop effective identification and accurate quantification of pathogenic bacteria [163,164,165]. Therefore, it is important to have reliable and sensitive methods to detect these bacterial contaminants in aquatic products.
Chattopadhyay et al. [166] prepared H. pylori antibody fluorescent probe (FCDs-Ab) to detect H. pylori effectively. Dehghani et al. [167] built a sensor which could be bound with C. jejuni membrane surface proteins, leading to specific interactions between the probe and the target bacteria. The limit detection of the sensor was 10 CFU/mL.
The detection of S. aureus contamination can be achieved in two ways: indirect detection and direct detection [168, 169]. Ravikumar et al. [170] developed an “On–Off–On” fluorescent probe for the detection of micrococcus nuclease (MNase), which was the gold standard for identifying the presence and content of S. aureus. The detection limits for fluorescence-based strips and assay were 0.5 ng/mL and 0.3 ng/mL, respectively. For the detection of S. aureus enterotoxin A, Ma et al. [171] obtained lower background signal interference and lower detection limit (0.899 ng/mL) by centrifuging ssDNA attached GO.
Duan et al. [172] and Chinnappan et al. [173] used full-length and truncated fluorescent labelled aptamers to detect S. Typhimurium, respectively, and the results showed that the detection limit of the latter (25 CFU/mL) was much lower than that of the former (100 CFU/mL). Compared with these two studies, Renuka et al. [174] utilized QDs-modified aptamers, which had a lower detection limit (10 CFU/mL). Satisfactorily, this sensing platform had no cross-reaction with other similar bacteria. Through the comparison of the above three studies, it can be found that the length of aptamer and the type of fluorescent substance used for labelling will affect the evaluation accuracy.
In order to detect A. baumannii, Xie et al. [175] developed a sensor based on a DNA-catalyzed amplification mechanism (with a detection limit of 1.1 CFU/mL). A. baumannii could be bound with aptamer, causing the release of the template strand, which triggered an entropy-driven catalysis (EDC) reaction. Then, one product of EDC was used as the catalyst for catalytic hairpin assembly (CHA) on a GO nanosheet, leading to lots of FAM-labeled DNA duplicates released from GO, which could be detected with fluorescence intensity change. Besides normal fluorescent sensors, the ratiometric fluorescent sensor and the multicolour time-resolved fluorescence (TRF) sensor have also been applied in the detection system. Bahari et al. [176] reported an ingenious ratiometric fluorescent sensor based on nitrogen-doped carbon nanodots together with ortho-phenylenediamines carbon dots and GO. The sensor had a detection limit as low as 3.0 × 10−2 CFU/mL and was confirmed to detect A. baumannii in urine samples with satisfactory results.
The time-resolved fluorescent sensor is a promising tool for food safety control and inspection [177]. Huang et al. [178] established a TRF sensor for the evaluation of multiple S. aureus enterotoxins (SEs) simultaneously, including SEA, SEB, and SEC1. Each aptamer was labelled with a specific combination, which emitted unique fluorescence signals when bound to their respective SE toxin targets. Time-resolved detection reduced background noise and enhanced detection sensitivity. The sensor successfully performed the detection of milk samples with a detection limit of 0.020 to 0.068 ng/mL. The TRF sensor is a promising tool for food safety control and inspection [179].
Mycotoxin
Aflatoxin (AF) is a bifuran ring toxins produced by some strains of Aspergillus parasiticus and Aspergillus flavus, which is carcinogenic, immunogenic and teratogenic to human beings and animals [180]. There are a wide variety of aflatoxins, with about 20 structurally related compounds. Among them, aflatoxin B1 (AFB1), aflatoxin B2 (AFB2), aflatoxin G1 (AFG1) and aflatoxin G2 (AFG2) are the major aflatoxin metabolites associated with human and animal disease [181]. Besides, lactating animals can metabolize AFB1 to AFM1 and AFM2 by taking contaminated feed, presenting a risk to humans [182]. Zhang et al. [183] developed a novel method for simultaneous separation and measurement of AFM1 by synthesizing r-GO decorated by monoclonal antibody functionalized Fe3O4. Under optimized conditions, the quantitative and visual detection limits of AFM1 were 3.8 ng/L and 50 ng/L, respectively. These results demonstrated the high sensitivity and selectivity of this newly developed method for detecting the presence of AFM1.
In several AFB1 detecting studies [31, 106, 107, 184, 185] achieved lower detection by eliciting two fluorophore-labeled hairpin probes (HP1/HP2) and specific apt sensor with internal complementary sequence, respectively(0.03 pg/mL and 0.03 pg/mL). Although these methods exhibit sensitivity and specificity, there is still room for improvement in terms of speed, simplicity, and cost-effectiveness [186]. Future research may focus on developing portable, real-time, and multiplexed detection systems for aflatoxins, which will enhance food safety control and public health protection [187].
Ochratoxin is another mycotoxin that has attracted worldwide attention after aflatoxin, including 7 compounds with similar structures. Among them, ochratoxin A (OTA) has the highest content and the strongest toxicity [188]. Zhang et al. [109] and Wu et al. [189] realized sensitive detection of OTA (0.02 ng/mL and 11 pg/mL respectively). Besides, the platform built by Wu could also be used for assessing fumonisin B1 with a low detection limit (0.1 ng/mL).
Hazardous Endogenous Substances
Allergen
To date, effective medical treatment has not been found for food allergies [190]. The only possible method of prevention may be to rely heavily on avoiding foods containing specific allergens altogether [191]. Figure 4 describes the schematic diagram of the food anaphylactic reaction. The major allergens of aquatic species include tropomyosin (TM) and arginine kinase (AK) [192]. In general, allergenic components of aquatic products can cause allergic reactions ranging from mild to life-threatening when they come into contact with the mucosal immune system in the gut [111].
Schematic diagram of food anaphylactic reaction
TM is a major allergenic protein found in invertebrates such as shrimps and crabs, whose structure remains highly stable even in high-temperature environments [193]. Zhang et al. [194] designed a labelling-free TM fluorescent biosensor based on GO and OliGreen labelled aptamers. The aptamers obtained by SELECT showed high affinity for TM, and could selectively recognize TM across a broad concentration range. The detection limit for TM evaluation was 4.2 nM, and the range of detection was from 0.5 to 50 µg/mL in binding buffer solution. For the purpose of further improving detection accuracy, Chinnappan et al. [110] used a minimal-length aptamer sequence with fluorescein at the 5’end to build an evaluation platform based on GO. The result eventually confirmed that the detection limit was as low as 2.5 nM, which was significantly lower than that of the full-length aptamer sequence. Meanwhile, the reaction could be finished within 30 min. The detecting platform proved that truncated aptamers could form unique secondary structures to capture TM with higher affinity. After mixing shrimp TM into chicken noodle soup purchased at a local market, the authors detected the sample and verified the feasibility of the detection sensor.
AK is a kind of guanidine phosphate compound kinase found in invertebrates, which is regarded as one of the main shellfish allergens [114]. To achieve sensitive and swift quantitative detection of AK, Zhou et al. [195] used carboxyl functionalized CQDs to modified aptamers, and constructed an “On-Off-On” fluorescent aptamer biosensor based on GO, providing a detection limit as low as 0.14 ng/mL.
Biotoxins
In the area of biotoxin detection, several studies have been conducted to develop innovative methods for detecting various toxins [196]. Microcystin (MC) is a potentially harmful toxin found in aquatic systems and has been identified as a potent hepatotoxin and tumour promotor [116]. Shi et al. [108] established a reliable MC biosensor by using gold nanoparticles (AuNPs), which met the WHO guidelines for detecting MC-RR and MC-LR (0.3 µg/L and 0.5 µg/L separately). Gu et al. [197] conducted the first study that used GQD-labeled aptamers and DNase I-catalyzed amplified target circulation signals to detect marine organisms. To achieve sensitive and rapid detection of saxitoxin (STX), the authors employed magnetic r-GO as an energy receptor, STX-41 aptamers as a recognition element, GQDs as fluorescence signal, and DNase I for enzymatic signal amplification. They successfully detected STX with a broad detection range of 0.1 to 100 ng/mL and a detection limit as low as 0.0035 ng/mL under optimized conditions. Kweon et al. [115] constructed an okadaic acid fluorescent biosensor with satisfactory specificity recognition compared to other marine toxins, whose detection limit was 6.35 ppb.
Advantages, Challenges and Future Works
With the continuous improvement of global consumption demand for aquatic products, aquatic product safety control is becoming a tough problem gradually. The requirement for efficient, rapid and low-cost detection methods is increasing as well [198]. At present, GO/r-GO fluorescent sensors have made some progress in aquatic food safety detection, especially compared with traditional detection methods, they have several outstanding advantages as shown in Fig. 1, which are mainly reflected in four aspects. However, there are certain challenging issues that should be addressed to facilitate future developments, indicating that more efforts should be made in future.
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Currently, graphene and its derivatives are predominantly used in applications such as display screens, conductive devices, and thermal conductive devices. Although graphene’s excellent electrical conductivity has made it useful for biosensing, its unique optical properties have yet to be extensively explored in this regard. Additionally, most research on fluorescent sensors has focused on GO rather than r-GO. However, the sensitivity of fluorescent sensors is closely related to the substrate’s fluorescence quenching ability. As r-GO has shown better quenching ability than GO, further exploration is needed for the development of r-GO-based fluorescence sensing systems.
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The preparation of r-GO typically involves chemical reduction, and consuming hydrazine and other toxic chemicals. Not only can this be harmful to human health, but it also poses a significant threat to the environment. Therefore, future work can focus on exploring green and efficient GO reduction methods. One potential approach is to improve plasma treatment technology, which can reduce GO under specific gas (methane, argon, NH3, etc.) or liquid (alcohol) environmental conditions. This method offers advantages such as high speed, controllability, high yield, and low cost [70, 83, 199].
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The large-scale commercial production of aptamers is currently not feasible, and their relatively weak affinity and selectivity in real samples greatly limit their application. As a result, only a few aptamers have been fully validated and widely used. To address this limitation, greater efforts should be directed towards improving the sensitivity and specificity of aptamers. Promising approaches include structure optimization, function improvement, truncation of non-essential parts, and combined use of aptamers [200].
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There are still certain gaps in aquatic food safety detection using GO/r-GO fluorescent sensors. The range of detectable substances is not sufficiently diverse, which prevents the establishment of a comprehensive detection system. Future research should focus on expanding the detection capabilities to include more harmful substances and improving the overall detection system for aquatic products.
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Looking ahead, the attempts to explore potential synergies between GO/r-GO sensors and other emerging technologies, such as microfluidics and surface-enhanced Raman scattering sensors, could lead to the development of integrated systems for comprehensive real-time monitoring of food safety parameters, facilitating their development in commercial applications [201].
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All in all, while challenges remain in the development and adoption of GO/r-GO fluorescence sensors for aquatic food safety testing, the field holds great promise in revolutionizing food safety practices and ensuring the well-being of consumers worldwide. By addressing technology and commercialization challenges in a collaborative and interdisciplinary way, researchers and industry stakeholders can pave the way for a safer and more secure food supply chain.
Conclusions
The construction of fluorescent biosensors based on GO/r-GO with highly efficient fluorescence quenching performance is presented. Its application in aquatic food safety detection is also discussed, mainly focusing on three aspects, including the detection of harmful chemicals, harmful microorganisms and their toxins, and endogenous harmful substances. The sensitivity of aptamers, fluorescence labelling performance and fluorescence quenching ability of substrate are the main factors affecting the detection sensitivity of GO/r-GO fluorescent sensors. Future research should focus on further exploration in the above three aspects, such as improving green and safe graphene oxide reduction technology, exploring and using more sensitive aptamers or truncated aptamers, and laying a research foundation for the industrial production of such detection sensors. In conclusion, the construction of fluorescent sensors will be the mainstream trend of future detection development. Hopefully, this review will encourage further research, and explore more applications of r-GO optical properties in food detection.
Data Availability
The authors are unable or have chosen not to specify which data has been used.
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Acknowledgements
The authors are grateful to the National Natural Science Foundation of China (32272466) for its support. This research was also supported by Guangdong Basic and Applied Basic Research Foundation (2021A1515010644, 2021A1515110396), Guangzhou Basic and Applied Basic Research Foundation (202201010008), the Contemporary International Collaborative Research Centre of Guangdong Province on Food Innovative Processing and Intelligent Control (2019A050519001), and the Common Technical Innovation Team of Guangdong Province on Preservation and Logistics of Agricultural Products (2023KJ145).
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Chen, MX., Cheng, JH., Ma, J. et al. Advancing Aquatic Food Safety Detection Using Highly Sensitive Graphene Oxide and Reduced Graphene Oxide (GO/r-GO) Fluorescent Sensors. Food Eng Rev (2024). https://doi.org/10.1007/s12393-024-09375-5
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DOI: https://doi.org/10.1007/s12393-024-09375-5