Current Trends in Detection of Histamine in Food and Beverages

Review Cite This: J. Agric. Food Chem. 2019, 67, 773−783

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Current Trends in Detection of Histamine in Food and Beverages Milica Gagic,†,‡ Ewelina Jamroz,§ Sona Krizkova,†,‡ Vedran Milosavljevic,†,‡ Pavel Kopel,†,‡ and Vojtech Adam*,†,‡ †

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Department of Chemistry and Biochemistry, Faculty of AgriSciences, Mendel University in Brno, Zemedelska 1, CZ-613 00 Brno, Czech Republic ‡ Central European Institute of Technology, Brno University of Technology, Purkynova 123, CZ-612 00 Brno, Czech Republic § Institute of Chemistry, University of Agriculture in Cracow, Balicka Street 122, PL-30-149 Cracow, Poland ABSTRACT: Histamine is a heterocyclic amine formed by decarboxylation of the amino acid L-histidine. It is involved in the local regulation of physiological processes but also can occur exogenously in the food supply. Histamine is toxic at high intakes; therefore, determination of the histamine level in food is an important aspect of food safety. This article will review the current understanding of physiological functions of endogenous and ingested histamine with a particular focus placed on existing and emerging technologies for histamine quantification in food. Methods reported in this article are sequentially arranged and provide a brief overview of analytical methods reported, including those based on nanotechnologies. KEYWORDS: histamine, biogenic amines, food safety, analytical chemistry

1. INTRODUCTION Biogenic amines are nonvolatile, heat-stable bases with biological activity having aliphatic, aromatic, or heterocyclic structures.1 They are the result of metabolic activity in plants, animals, and humans and are usually formed by the decarboxylation of amino acids. The human body naturally produces biogenic amines, which are synthesized through cellular metabolism having diverse physiological functions. Some of them act as hormone mediators or neurotransmitters, while others are precursors of hormones, proteins, alkaloids, and nucleic acids.2 Histamine is a biogenic amine synthesized from the histidine through the catalytic activity of histidine decarboxylase.3 This molecule comprises an imidazole ring and an aliphatic amino group connected by a two-carbon-atom chain. The amino and imidazole groups are both basic and are protonated in acidic solution. Under physiological conditions, histamine is mainly protonated at the aliphatic amino group (96%), with minor dicationic (3%) and neutral forms (1%).4 The aim of this review is to provide background knowledge for studying histamine, which is important for food safety with a special focus on new and emerging techniques of histamine detection. 1.1. Physiological Roles of Histamine. Histamine is a conserved autacoid distributed widely throughout the body and is found in most vertebrate tissues. It is a ubiquitous biogenic amine, produced and stored in conjugation to heparin in mast cells and basophils. Nonmast cell histamine is known to be localized in gastric enterochromaffin-like cells and in varicosities of the histaminergic neurons.5,6 Histaminergic neurons, exclusively growing within the posterior hypothalamic tubero-mammillary nucleus, project diffuse varicose fibers to the entire central neural system (CNS). These neurons are mostly unmyelinated and form few synaptic junctions mainly onto dendritic shafts. Histamine biosynthesis and secretion in the brain are under negative feedback by histamine autoreceptors on an axon terminal of histaminergic neurons.7 © 2018 American Chemical Society

It is known to play a role in the modulation of circadian rhythms as well in regulation of cognitive motor and sleep behavior.8 Moreover, histamine is localized in specialized cells in the gastric mucosa called enterochromaffin-like cells. These cells respond readily to hormonal and neural stimuli with histamine release, which further catalyzes the formation of intracellular messengers and controls gastric acid secretion.9 Histamine plays a key effector role over numerous pathophysiological functions, but so far, it is mainly recognized for its well-established effect in allergic inflammatory reactions. Histamine release leads to the activation of mast cells and basophils by several mechanisms, as this results in the symptoms of allergy and anaphylaxis. During an inflammation, when the process is initiated by an allergen, a specific immunoglobulin E (IgE) molecule is produced against the particular antigen.10 Consequently, histamine is unfastened by activated mast cells and as an effector molecule induces allergic or inflammatory reactions or modulates innate and adaptive immune response.11 Histamine, moreover, stimulates different biological responses through tissue-specific expression of four major subtypes of receptors. The pathogenesis of allergic reaction is mediated via the H1 receptor. The main effects of H2 receptor stimulation result in gastric acid secretion. The H3 receptor is a presynaptic autoreceptor regulating a neural activity in the brain.12 Subsequently, it is shown that H3 also modulates levels of other important neurotransmitters via a parallel role as a heteroreceptor in the CNS.13 H4 receptors are expressed in hematopoietic and immunocompetent cells and mediate eosinophil cell shape change and mast cell chemotaxis.14 All histamine receptors transfer the hormonal signal through Received: Revised: Accepted: Published: 773

October 9, 2018 December 4, 2018 December 25, 2018 December 26, 2018 DOI: 10.1021/acs.jafc.8b05515 J. Agric. Food Chem. 2019, 67, 773−783

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Journal of Agricultural and Food Chemistry

Figure 1. Scheme of the signal transduction pathways via histamine receptors and their physiological functions modified according to Panula et al.6 For more detailed information see section 1.2 or the review by Panula et al.6

fermented food such as sauerkraut, beer, and wine.20 It does not usually represent any health hazard. Nevertheless, when food is rotten, the amount of histamine increases to a toxic level (50 mg/100 g of the food), which causes food poisoning.21 This can be accompanied by the occurrence of bacterial species Morganella psychrotolerans, Morganella morganii, Klebsiella pneumoniae, and Proteus vulgaris in spoiled scombroid fish, where elevated production of histamine was evidenced.22 Formation of biogenic amines in food has been prevented traditionally by limiting microbial growth through chilling and freezing. When this approach is not sufficient or applicable, prevention of biogenic amine formation or reduction in their levels may be provided by alternative approaches such as hydrostatic pressures, irradiation, controlled atmosphere packaging, food additives, and spices. Histamine can also be degraded by bacterial amine oxidases, diamine oxidase (DAO), or amine-negative bacteria that are added to starter cultures for fermentation.23 Histamine in the human gut is rapidly metabolized by intestinal DAO to less active products.24 If the detoxification system is not able to eliminate ingested histamine, it binds to specific receptors, causing symptoms generally similar to those of IgE-mediated food allergies.25 Typical symptoms of histamine intoxication are nausea, sweating, headache, and hyper- or hypotension.26 A high concentration of histamine is found in foods with proteins and free amino acids which readily undergo microbial decarboxylation. Factors which govern the formation of histamine in food are the presence of free amino acids and microorganisms producing decarboxylases under felicitous conditions for their growth. Histamine poisoning, also known as scombroid fish poisoning, was previously connected with eating a type of fish containing high levels of histidine in its muscular proteins. However, it was discovered that this poisoning was due to particular autolytic proteases produced by contaminant bacteria.27 These enzymes break down proteins in spoiled

coupling with specific G proteins. Particularly, an activation of the H 1 receptors coupled to G q proteins stimulates phospholipase C activity. This results in the formation of 1,2-diacylglycerol (DAG) and inositol-1,4,5-triphosphate (IP3) with a consequent increase in intercellular calcium concentration. A higher level of cytosolic Ca and protein kinase C, which is activated by DAG, is responsible for a wide variety of pharmacologic effects of H1 receptor stimulation.15 H2 receptors activate Gαs, triggering adenylyl cyclase activation and enhanced cAMP formation which leads to different downstream cascade effects.16 Activation of the H3 receptor leads to inhibition of cAMP formation, activation of PI3K pathways, and subsequent activation of another ubiquitous signaling molecule, protein kinase B. The H4 receptor is mostly expressed on the surface of immune cells and, like the structurally related H3, is mainly coupled to Gi/o proteins. Stimulation of the H4 receptor leads to inhibition of forskolininduced cAMP formation and enhanced calcium influx as well as MAPK activation by direct coupling to β-arrestins (Figure 1). 1.2. Metabolism. Histamine is formed from the histidine precursor via oxidative decarboxylation mediated by an enzyme called histidine decarboxylase (HDC). There is no other enzymatic pathway for histamine generation, and this enzyme is produced by many cells in the body. Only 2−3% of histamine is released unchanged. The rest of the histamine is metabolized by other mechanisms. Histamine can be catabolized by deamination via diamine oxidase (DAO) to form imidazole acetaldehyde or methylation by histamine Nmethyltransferase (HMT) to produce methylhistamine.17 The last pathway is acetylation by acetylase to 4-(βacetylaminoethyl)imidazole, but this process was observed only for enterobacteria.18,19 1.3. Histamine in Food. Despite its known regulatory function in human physiological processes, low histamine concentrations occur naturally in food and drinks, especially seafood, ripened cheese, some fruits and vegetables, and 774

DOI: 10.1021/acs.jafc.8b05515 J. Agric. Food Chem. 2019, 67, 773−783

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Journal of Agricultural and Food Chemistry fish, therefore releasing free histidine. The consumption of spoiled fish leads to the development of histamine poisoning, but the measurement of the minimal toxic levels of histamine is very difficult. The dose-dependent toxicity of histamine varies among individuals, and it relies on the detoxification efficiency of each individual.28,29 Various hypotheses were sought to determine the mechanism, which causes histamine toxicity. The current accepted opinion is that histamine is not the only factor causing intoxication but is potentiated by some other component.19 The presence of a second amine can raise the toxicity of histamine by inhibition of intestinal histamine metabolizing enzymes, increase of histamine uptake, and liberation of endogenous histamine in intestinal fluids.30 Nevertheless, there is no clear understanding of how these synergistic effects occur and the pathogenesis of histamine fish poisoning still needs to be clarified. In individuals with histamine intolerance or hypersensitivity, foods with a high content of histamine should be excluded from the diet or consumed moderately. The symptoms of histamine poisoning may occur after the ingestion of 0.75 mg/ kg body weight of histamine or a food containing 50 mg/kg of histamine in predisposed individuals,24,31 while according to European Commission Regulation (EC) No. 2073/2005 on microbiological criteria for foodstuffs, the limit of histamine content in fresh fish of species associated with increased levels of histidine (particularly Scombridae, Scombresosidae, Engraulidae, Coryfenidae, and Pomatomidae Clupeidae families) is less than 100 mg/kg; in fermented fish products from those families it is less than 200 mg/kg and less than 400 mg/kg for fish sauce.32,33 Serum DAO activity is used for monitoring of histamine hypersensitivity,34 when DAO supplementation is helpful for managing histamine intolerance in some cases. However, multiple mechanisms of histamine production and/ or degradation in the body make serum DAO activity and DAO supplementation unreliable. 35,36 In some foods, especially fish and fruits, the histamine level may vary based on their origin, cultivar, storage, and planting conditions; therefore, diligent control of food freshness and origin is necessary together with empirical finding of tolerated food. For example, absolutely fresh tuna meat can be consumed by a histamine-intolerant individual, as histamine levels are usually below 1 mg/kg,22 while the tuna meat after 5 days of storage at a very low temperature (0−2 °C) with a short period of inappropriate storage may cause health problems due to the increased histamine content.37 On the basis of the aforementioned facts it can be concluded that histamine detection and determination is very important for the food industry and food safety (Figure 2). This review further summarizes methods and procedures employed for detection/determination of this molecule, where we highlight both standard and trend approaches.

2. HISTAMINE DETECTION A plethora of techniques have been described to provide information about the levels of histamine in different sorts of food (Figure 3). Due to the complexity of the matrix sample, extraction of histamine from food samples presents a significant challenge to sample processing. Many different analytical methods have been investigated; for an overview see Table 1. A review by Onal from 2007 provides a great insight into various approaches to biogenic amines determination in food.28 Later especially chromatographic approaches to histamine detection in food and beverages together with other biogenic amines were reviewed several times: for example Lazaro de la Torre et al. in 2013, who focused on chromatographic methods for determination of biogenic amines in foods of animal origin,38 Sentellas et al. in 2016, who summed up the advances on determination of biogenic amines in food samples by (U)HPLC),39 Ordonez in 2016, who summarized recent trends in determination of biogenic amines in fermented beverages,40 Mohammed et al., who gave an overview of the chemistry, cleanup, and advances in analysis of biogenic amines in foodstuffs in 2016,41 and Papageorgiou et al., who updated the knowledge about analytical methods for determination of biogenic amines in food and beverages in 2018.20 To our knowledge, no work aimed at entirely histamine that includes also emerging and nanotechnologybased methods has been published. In the following chapters and subchapters we provide an overview of the situation in single approaches over the past decade. 2.1. Colorimetric and Fluorometric Analysis. Many of histamine assays in food samples have been set up in early days of modern analytical chemistry and relied on pioneer work on colorimetric or fluorometric analysis. Colorimetric determination of histamine in animal tissues, published in 1955, is based on the reaction of histamine with an aromatic diazo compound as a coupling reagent and measuring the product spectrophotometrically at 495 nm.42 However, the reaction is not very specific; therefore, purification of histamine by the use of carboxylic cation exchangers is necessary to exclude interfering compounds. In 1994, Bateman described a method based on the reaction of purified histamine with copper and a dye, which determines histamine levels in yellowfin tuna steaks.43 He avoided covalent derivatization of histamine but reported its strong chelating properties. The colorimetric method reported by Patange and his team in 2004 appeared to be simple, inexpensive, and rapid for determination of histamine concentration in fish meat.44 Quantitative measurement of histamine was done via interaction between pphenyldiazonium sulfonate and the imidazole ring. The concentration of histamine is determined by visual comparison of the color intensity of the sample with that of a histamine standard, at six different concentrations. Although the assay is simple and requires no laborious treatments, it is not often used because it is semiquantitative and cannot be used beyond a certain concentration. Other methods have been developed to tackle the low sensitivity and specificity of the colorimetric methods. As histamine is a non-UV-absorbing analyte and has no native fluorescence, chemical derivatization is necessary to form detectable substances.45 The first fluorimetric test for histamine analysis in animal tissues was developed in 1959 by Shore and co-workers.46 Although the results for histamine concentration were distorted by interfering substances, the test revolutionized the analysis of histamine in biological samples.

Figure 2. Chemical formula of histamine (left) and schematic illustration of importance of histamine analysis in food (right). 775


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Figure 3. Summary of common and emerging histamine detection techniques.

Table 1. Summary of the Existing Methods for the Determination of Histamine in Food sample

separation method

detection

LOD

ref

yellowfin tuna fish canned tuna fish cheese fish commercial fish fish baby foods cheese fish fish fish beer seafood various food canned tuna canned fish fish and squid fish samples fish samples chicken meat fish fish samples ham various food fish sauce tuna fish canned tuna liquid tuna fish fish fish red wine canned tuna seafood fish meat fish

IEC IEC IEC GC UHPLC LC HPLC TLC HPLC GC FIA Paper electrophoresis IEC CZE ELISA UA-CPE MIP HS-SPME TLC DAO/HRP/ferrocene MAO/HRP/ferrocene MAO/MnO2 opper electrode nanocomposite films/HA-Ag boron-doped diamond electrode IEC rhenium dioxide/carbon electrode CHI/MIPs MIPs CdTe QDs HB@NPS@FC AuNPs GNR-AgNPs Cu@Pd nanoporous alumina membrane/MNP AMPNi/GE microfluidic-chip system/HPLC microchip electrophoresis

copper chelation assay, UV 515 nm visible color change between histamine and p-phenyldiazonium λex/λem 450/360 nm MS UV 254 nm MS/MS λex/λem 330/520 nm densitometry APCI/MS MS λex/λem 365/450 nm color developing with Pauly’s reagent conductometric detection λex/λem 417/440 nm colorimetry FAAS SERS MIR-IMS UV 330 nm amperometric amperometric amperometric amperometric amperometric SWV conductometry amperometric UV 468 impendance spectroscopy λex/λem 365/450 nm FRET/λem 526 nm UV 522 nm SWV amperometric electrochemistry electrochemistry UV 440 nm C4D

0.125 mg kg−1 10 mg kg−1 50 mg kg−1 50 mg kg−1 1 mg kg−1 0.05 mg kg−1 0.24 mg kg−1 20 mg kg−1 1.4 μg kg−1 10 mg kg−1 6 mg kg−1 15 mg kg−1 0.45 mg kg−1 0.61 μg L−1 0.9 mg kg−1 2.5 μg kg−1 3 mg kg−1 0.6−1 mg kg−1 1 mg kg−1 0.17 mg kg−1 8.88 μg kg−1 3.3 mg kg−1 0.08 mg kg−1 0.04 mg kg−1 3−9 mg kg−1 2.44 mg kg−1 0.2−0.3 mg kg−1 1.5 mg kg−1 0.1 mg kg−1 1.1 mg kg−1 0.188 mg kg−1 0.7 μg kg−1 5.44 μg L−1 0.17 μg kg−1 0.66 μg kg−1 2.82 μg kg−1 40 μg kg−1 2.15 mg kg−1

43 44 47 48 53 71 119 49 78 77 56 57 58 59 60 62 63 64 66 86 84 88 96 95 89 90 92 105 98 106 108 109 113 114 111 112 118 117

most promising quantitative method for histamine analysis, but currently, major parts of the methods rely on chromatographic separation. Since the 1980s, thin-layer chromatography (TLC), gas chromatography, high-performance liquid chromatography (HPLC), and ultrahigh-performance HPLC (UHPLC) coupled to various detectors have been commonly used to determine histamine levels in foods.48−54 The literature includes other methods for histamine detection such as ion chromatography, capillary electrophoresis, paper electropho-

The method was based on the reaction between OPT and histamine and measurement of the intensity of the resulting fluorescent conjugate. Later, many scientists have attempted to overcome the limitations of this method. Modifications involving IEC to remove accompanying substances by Lerke and Bell, in 1976, proved to be more successful, and they reported an assay directly applicable in fish.46,47 2.2. Separation Techniques. The aforementioned scientists unquestionably set up a fluorimetric method as the 776


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fluorescent isoindole compound.70 In the same year, Sagratini et al. proposed and described a method for direct analysis of eight biogenic amines in fish avoiding derivatization;71 however, the detection of “bare” biogenic amines, due to their high polarity which often causes weak interaction with a C18 stationary phase, is still a great challenge for researchers. Ultrahigh-performance liquid chromatography (UHPLC) in connection with either fluorescence or UV detection with either precolumn or postcolumn derivatization allows the detection of biogenic amines with LOD values on the order of hundreds of μg/kg;39 for example Š imat et al. obtained a detection limit of 200 μg/kg for histamine in a seafood matrix.72 UHPLC and high-resolution mass spectrometry (UHPLC-HRMS), most frequently coupled with a TOF or Orbitrap analyzer, with an LOD as low as units of μg/kg offer great possibilities for the determination of biogenic amines in food matrices serving either for their determination in food or for food characterization through compositional profiles:39 for example, Self et al. obtained an LOD of 1.57 μg/kg in a fish matrix.73 Following fluorescence detection, a novel method allowing diagnosis of histamine intolerance by histamine and methylhistamine detection in urine by ultrahigh performance liquid chromatography coupled with fluorimetric detector (UHPLC-FL) was developed in 2017.74 An HPLC method from 2018 with fluorescence detection allowed the determination of histamine together with nine other biogenic amines after derivatization with dansyl chloride with linearity in the range 0.25−10 μg/mL and a detection limit of 75 ng/mL for histamine in rat plasma.75 Coupling HPLC or GC with mass detection allows a decrease in the detection limit of histamine even more. After derivatization and microextraction followed by GC, it was possible to detect histamine in nine different seafood and salami samples and the concentration ranged from 5.19 to 817.3 mg/kg, which meets the requirements of food quality surveillance posted by legal authorities.76 An IBCF (isobutyl chloroformate) derivatization and microextraction method followed by gas chromatography−mass spectrometry (GC-MS) was applied to extract four biogenic amines, including histamine, from Iranian Lighvan cheese samples with a detection limit of 10 ng/g for histamine.77 Simultaneous determination of six derivatized biogenic amines from baby food is easily achieved (with a detection limit of 0.07 ng/mL for histamine) using HPLC coupled with single-quadrupole mass spectrometry (HPLC-APCI-MS).78 Ultra-HPLC coupled with a single-stage high-resolution mass spectrometer (Orbitrap) allowed the detection of 10 biogenic amines with a limit of quantification for histamine of 5 mg/kg in fish meat.79 2.3. Biosensors. The application of biosensors for biogenic amine analysis is a good alternative to traditional methods for its decreased costs, rapidity, ease of use, and no need for bulky instruments and skilled operators.80 Since Lerke introduced the first enzyme assay in 1983 for histamine monitoring, extensive studies based on enzyme dependent reactions have been carried out.81 Lerke used a two-step sequential enzyme system to determine histamine in raw and canned tuna flesh. The resulting hydrogen peroxide is determined by formation of crystal violet from the leuco base and should follow a linear relationship with the concentration of histamine.81 Due to the complex nature of the reaction, the obtained results were not as conclusive as was expected. The earliest example of a histamine amperometric device was demonstrated by Loughran in 1995 and later improved by Zeng and Bao in 2000.82,83 This gadget represents the first reported use of an enzyme-

resis, flow-injection analysis (FIA), enzyme electrodes, immunoassays, flame atomic absorption spectroscopy (AAS), Raman spectroscopy, and ion mobility spectrometry (IMS).55−64 The analysis of biogenic amines in food is, however, limited due to the complexity of the sample matrix and the low analyte concentrations in samples. To enhance the performance and to improve the detection and quantification limits of these methods, sample preparation and analyte preconcentration are almost always applied. Sample pretreatment is recommended to avoid interferences with complex food matrices either by removal of interfering compounds or by selective extraction of analytes. Since histamine does not contain chromophoric or fluorogenic moieties, derivatization is needed to improve detectability by spectroscopic or fluorometric detectors. In 1976 Schutz et al. were interested in scombroid toxicity and examined a number of TLC methods for their potential use as fast screening techniques for the determination of histamine in tuna extracts.65 One-dimensional TLC was carried out; 10 μL of sample was spotted on the plate. After development in a methanol/ammonia (20/1, V/V) mobile phase, the plate was dried and the histamine spot was treated with ninhydrin. Detection was done either quantitatively via densitometry or semiquantitatively by comparative analysis of color densities of the histamine spots between the sample and a standard reference of histamine, provided that the spots showed the same retardation factor values, on the chromatographic plate.65 Since then, a great number of new variants of the original method have been developed.50 In 2004, LapaGuimarães and Pickova introduced an improved system for TLC. By using a new solvent system, automated sample application apparatus, and a scanner with densitometric capabilities, they developed a more accurate analytical procedure for separation and quantification of nine biogenic amines in fish and squid.66 This methodology provides quantitative results similar to those from HPLC. The last TLC technique published allowed a low quantification (78.29 mg/spot) and detection limit (23.49 ng/spot) of histamine in fish after a chromogenic reaction of diazotized p-nitroaniline and the imidazole ring.67 Numerous HPLC methods have been designed for histamine detection and determination, but HPLC with C18 reversed-phase columns and gradient acetonitrile−water (65− 90% acetonitrile) mobile phase with a detection limit below 0.06 ppb reported in 1996 for detection of biogenic amines in food matrix (cheese, fish, and preserved meat), remains the technique of choice.68 Usually a precolumn or postcolumn derivatization process with a chromophore or fluorophore is needed for enhanced detection. Derivatization generally involves extensive sample preparation because derivatization agents can react with an undesired matrix constituent. As a result, the procedure may be very tedious and time-consuming. HPLC is a quantitative technique that is suited for online sample cleanup and is widely used as a method for histamine separation. When HPLC has been coupled with a variety of detectors, practically all biogenic amines have been separated and detected. Selected examples from the literature on HPLC-based separation are discussed. In 2012, histamine was isolated from meat and meat product samples by ion exchange chromatography and then derivatized with o-phthalaldehyde (OPA).69 OPA is one of the fluorogenic agents that reacts with primary amines in the presence of 2mercaptoethanol under basic conditions, producing a 777


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that enzyme is in close contact with both the analyte and the transducer and this immobilization process can have an influence on the enzyme stability and activity. This issue was solved by the development of molecular imprinting, which allows creating synthetic recognition sites with a predetermined selectivity and specificity for the desired analyte. Molecular imprinted polymers (MIP) are complementary to the template in their shape, size, and chemical functionality; thus, they are useful for the separation and analysis of complex matrices such as food samples and aqueous media. The basis of MIP preparation is conventional polymer chemistry. MIPs are synthesized by polymerization of a cross-linking agent with a complex of the precursor molecule and the functional monomers using chemical interactions. Removal of the precursor molecule leaves behind specific cavities that are able to recognize and bind selectively only the precursor molecules. MIPs are among the most rapidly developing strategies for detection of several analytes, including histamine as a target molecule.97 The method that utilizes MIPs for histamine detection has been reported by Horemans et al. An MIP-based recognition element was coupled to two different sensing platforms, piezoelectric and impedance transducers, for detection of histamine in aqueous media.98 The results showed that the piezoelectric sensor could be used to detect histamine in the micromolar concentration range. In addition, the impedance-based sensor detects the target molecule in the nanomolar range.98 Thermal detection of histamine with a graphene oxide based MIP platform (GO-MIP) was designed and applied for histamine sensing in buffer solutions.99 MIP films were also used for histamine detection by surfaceplasmon resonance (SPR),100 and MIP nanoparticle based potentiometric sensors were developed for histamine estimation in fish and wine.101 In the MIP-based fluorescent sensor for histamine the molecularly imprinted nanofiber served as a receptor and a CdSe/ZnS quantum dot (QD) was used as a signal transducer. QD-incorporated, histamine-imprinted organogels polymerized in situ were found to recognize histamine with high sensitivity and selectivity.102 Histamine MIPs were integrated into a carbon paste electrode as a biosensor platform for voltammetric detection of histamine. This biosensor allowed sub-nanomolar histamine determination in serum samples. This sensor was also tested for specificity in the presence of analogous molecules such as serotonin, dopamine, and others.103 A competitive fluorescent pseudoimmunoassay exploiting MIPs was developed for the determination of histamine and other biogenic amines in food matrixes by Mattson et al.104 Recently, Hashemi et al. employed a molecular imprinting technology to prepare magnetic MIP-Fe3O4 composites for recognition of histamine in real samples.105 These polymers can be easily collected and rapidly separated using an external magnetic field and have a large potential for the enrichment and separation of histamine from complex matrices. They developed a new approach for the preparation of MIP-coated magnetic nanoparticles by cross-linking of chitosan with (3glycidyloxypropyl)trimethoxysilane (GPTMS) in the presence of histamine as a template molecule. After separation, a spectrophotometric determination was carried out by a histamine reaction with 5,6-dicyano-p-benzoquinone (DDQ) reagent.105 Using magnetic MIPs allows the development of a highly selective and fast extraction procedure for detection of histamine in the nanomolar concentration range. The technology presented in this work is a promising substitute

based electrode. The success of enzyme-coupled electrochemical sensors is based on excellent enzyme specificity combined with the analytical precision of signal transduction after the biorecognition reaction. These biosensors are mainly based on amine oxidases. Amine oxidases constitute a class of enzymes that catalyze an oxidative deamination of primary amines with release of ammonia and H2O2. The consumption of O2 or the production of H2O2 is usually used for the quantification of biogenic amines in different food samples. The generation of H2O2 requires the use of a high potential, at which the effect of interferences present in samples is significant. One way to enhance the selectivity of the amperometric biosensor is to conjugate a secondary enzyme, peroxidase, leading to a bienzymatic sensor. This biosensor operates through peroxidase catalysis of the electrochemical reduction of H2O2, produced by amino oxidase, generated at a lower potential, where interferences are minimal.84 Electrocatalytic oxidation of histamine on a thin nickel electrode was employed to determine histamine chronopotentiometrically.85 The major types of the current histamine biosensors are based on electrochemistry and have been used for the detection of histamine in fish samples and for detection of meat spoilage.86,87 Another amperometric biosensor with amine oxidase (from pea seedlings) and a screen-printed carbon electrode, modified with MnO2, for determining biogenic amines (BAs) was developed with a limit of detection of 3 μM for histamine.88 Square-wave voltammetry was able to resolve the signals of cadaverine, histamine, putrescine, and tyramine in a mixture using a boron-doped diamond electrode.89 Ion chromatography with conductometric detection was proposed for the determination of biogenic amines including histamine in food samples including fish, smoked meat, and fruit.90 A competitive electrochemical immunosensor for histamine based on a graphene-coated electrode and horseradish peroxidase with a detection limit of 0.5 pg/mL was developed.91 The electrocatalyzed oxidation of histamine on heterogeneous carbon (carbon paste and screen-printed carbon) electrodes coated with rhenium(IV) oxide was reported for its flow-injection amperometric detection in fish samples.92 Amperometric biosensors quickly detect histamine with detection limits from 0.05 to 10 ppb.93 Diamine oxidase based electrochemical biosensors linked to magnetic particles were developed for the determination of cadaverine, putrescine, and histamine with enzymatic generation of hydrogen peroxide that was determined by three types of modified electrodes (HRP, Prussian blue, and Co(II) phthalocyanine).94 A portable amperometric immunosensor using a Prussian blue−chitosan−gold nanoparticle nanocomposite film able to detect 1.25 ng/mL histamine in fish samples was developed by Dong et al.95 A simple enzyme-free amperometric method suitable to detect 0.33 μM histamine by using surface oxide regeneration behavior on a copper electrode was suggested by Lin et al.96 2.4. Emerging Methods for Histamine Analysis. Although most of the methods rely on traditional techniques to provide information about histamine concentration in food, alternative strategies based on a biosensing approach are emerging. Nonenzymatic biosensors have been explored recently, and current research activity is mainly focused on nanotechnology and molecular imprinting to improve the analytical performance and robustness of biosensor devices. 2.4.1. Molecular Imprinted Polymers. The main issue in the design of recognition-based biosensor derives from the fact 778


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Journal of Agricultural and Food Chemistry for the frequently reported methods for histamine analysis and opens the door for further innovation using magnetic separation. 2.4.2. Micro- and Nanoparticle/Materials Based Devices. 2.4.2.1. Fluorescent and/or Visual Detection. In 2017, Khan et al. described the application of CdTe quantum dots capped with thioglycolic acid as a photoluminescent probe for histamine determination in tuna fish samples.106 The aforementioned scientists, under optimized conditions, showed that the analytical response of CdTe quantum dots due to quenching by histamine molecules was concentration-dependent and was described by the standard Stern−Volmer relationship. To our knowledge, this was the first study using QDs to quantify the amount of histamine in a food sample. Year after, Toloza et al. reported stronger and selective interaction between histamine and amino-functionalized graphene QDs in the presence of Cu2+, Fe3+, and Eu3+ ions, enabling histamine concentration in spoiled tuna fish samples to be determined at sub-micromolar levels.107 Another fluorescence biosensor based on histamine blue saturated in nanoporous silica nanoparticles and a surface coating with fluorescein isothiocyanate (HB@NPS@FC) was designed. This biosensor was found to be selective for histamine detection among other biogenic amines due to repulsive charges of FC and histidine. The self-catalytic reaction served as a FRET-based histamine screening system in real fish samples, which was capable of detecting ppm levels of histamine in fish flesh.108 A colorimetric approach for on-site monitoring of histamine based on negatively charged gold nanoparticles covered with citrate was reported. Under the experimental conditions histamine was electrostatically attached to the nanoparticles via the protonated imidazole ring, which led to citrate displacement because of the strong affinity between the gold nanoparticles and imidazole. This interaction was possible to observe as an aggregation and color change of the nanoparticles from red to blue. The minimal concentration visually detectable for histamine was 1.8 μM. Using photometric detection at 522 nm decreased the detection limit to 30 nM. This method was tested for real unspoiled fish samples.109 Modified carbon black was used as a label in a colorimetric onchip immunoassay of histamine, enabling visual detection of the signal on a nitrocellulose surface with an LOD of 8 μg/ mL.110 2.4.2.2. Electrochemistry. Electrochemical biosensor based on biofunctionalized nanoporous alumina together with magnetic nanoparticles (MNPs) was developed for histamine determination. MNPs modified with antihistamine antibodies were used to capture histamine and transfer them to an antibody-modified membrane. Histamine concentrated on MNPs was bound in the membrane nanopores through interaction between the antibody and histamine. This resulted in a blockade signal that was detectable by electrochemical impedance spectroscopy across the alumina membrane with an LOD of 3 nM. The function of this biosensor was tested on saury meat stored under frozen conditions.111 An electrochemical biosensor for ultrasensitive voltammetric detection of histamine by using a gold electrode coated with a microporous nickel film (AMPNi/GE) was designed. 112 Hydrogen evolution assisted electrodeposition was used for deposition of a nickel film on the electrode. This biosensor was able to detect histamine in the 10 nM to 80 μM range with a detection limit of 4.2 nM.112

Silver nanoparticles coated with a graphene nanoribbon (modified with pyrolytic graphite) was used as a sensor for voltammetric histamine detection in blood plasma and red wine.113 Cu@Pd core−shell nanostructures on a pencil graphite substrate were suggested for amperometric detection of histamine with a detection limit of 0.0032 μM. This sensor was capable of detecting histamine in unspoiled canned tuna, where a 52 μM histamine concentration was detected.114 Lowcost laser-scribed graphene electrodes consisting of locally available material were developed for reagent-free food safety sensing. To modify the biosensor, the graphene surface was coated with copper particles and diamine oxidase. This electrode was tested for amperometric detection of histamine with a lower detection limit of 11.6 μM. Application of the biosensor was tested on lactic acid bacteria fermented fish paste. Prior to fermentation the levels of biogenic amines were below the limit of detection, and after fermentation the histamine content was found to be 19.24 ± 8.21 mg of histamine/kg, validating the applicability of the sensor for a food matrix.115 2.4.2.3. Microfluidics and Sample Preconcentration. Structured paramagnetic microparticles composed of a maghemite (γ-Fe2O3) core functionalized with tetraethyl orthosilicate or chitosan covered with Dowex were applied for the collection of biogenic amines from urine with consequent detection with ion-exchange liquid chromatography.116 Microchip electrophoresis with capacitively coupled contactless conductivity detection was used for the direct determination of histamine in fish flesh with a detection limit of 0.43 mg/L.117 Electromembrane extraction of biogenic amines in food through a microfluidic system with dabsyl derivatization and HPLC allowed simultaneous detection of as low as 3 μg/L of five biogenic amines (histamine, spermidine, cadaverine, putrescine, and tryptamine) inside sausage and kielbasa samples.118

3. CONCLUSION According to the World Health Organization histamine has been implicated as the causative agent in many food poisoning outbreaks. As the hazardous level of histamine does not affect organoleptic characteristics of the food, chemical analysis of foods for traces of this potentially hazardous compound is more than necessary. Even though the number and diversity of methods described for laboratory histamine testing are impressive, none of them have been specifically developed for the detection of histamine in all foods. This is mainly due to the inherent complexity of food samples and challenging analysis of these matrices. The discussed techniques perform adequately, but many of them are lacking rigorous validation studies and interlaboratory comparisons to firmly establish them as reference methods. The current legal requirement demands the separation of histamine using an anion exchange column, derivatizing the histamine with o-phthalaldehyde, and measuring the fluorescence of the resulting compound. Although this method has been validated by collaborative studies, it is complex and timeconsuming. With few exceptions most histamine analyses, from early techniques based on TLC to more powerful techniques such as HPLC, have been performed in laboratories with sophisticated equipment and only a limited number of samples can be tested. Early detection of unsafe levels of histamine is one of the best strategies in the prevention of problems related to this 779


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CZE, capillary zone electrophoresis; ELISA, enzyme-linked immunosorbent assay; FAAS, flame atomic absorption spectrometry; UA-CPE, ultrasonic-assisted cloud point extraction; SERS, surface-enhanced Raman spectroscopy; HS-SPME, headspace solid phase microextraction; MIR-IMS, modified ionization region ion mobility spectrometry; MIP, molecularly imprinted polymers; MS/MS, tandem mass spectrometry; SPE, screen-printed electrode; DAO, diamine oxidase; HRP, horseradish peroxidase; MAO, monoamine oxidase; MnO2, manganese dioxide; HA-Ag, histamine ovalbumin conjugate; SWV, square wave voltammetry; CHI/MIPs, chitosan molecularly imprinted polymers; AuNPs, gold nanoparticles; GNR, graphene nanoribbons; AgNPs, silver nanoparticles; Cu@Pd, copper core with palladium shell; HB@NPS@FC, histamine blue doped in nanoporous silica and surface modification with fluorescein; FRET, fluorescence resonance energy transfer; MNP, magnetic nanoparticles; AMPNi/GE, gold electrode modified with activated microporous nickel; C4D, capacitively coupled contactless conductivity detection

foodborne illness. As the symptoms can develop quickly after consumption of contaminated food, an accurate, on-site, and easy-to-use test is crucial. Test strips based on histamine dehydrogenase catalyzed oxidation of histamine are commercially available, giving a yes/no result after 10 min on the basis of the color development of both the test line and control line. Despite their practical use, this technology suffers from limited sensitivity and subjective test result interpretation and still needs further improvements. The detection and quantification of histamine continue to rely on conventional techniques. While these methods can be sensitive, they are greatly restricted by assay time. Furthermore, these methods are based on a spectroscopic or fluorometric determination, and so the number of screened samples is limited. Nevertheless, these limitations can be overcome by some other histamine detection techniques such as LC-MS, which eliminates the need for derivatization of histamine. However, their wide-scale application is still limited by complex instrumentation and time consumption. Hence, recent innovations in nanotechnology and the development of advanced detection methods with nanobased materials are essential for improvement of histamine testing. Due to the unique properties of nanoscale materials, they can be tailored to enhance sensitivity and reduce the detection time of analytical methods. The possibility of nanomaterials to be simply functionalized was used for histamine binding with appropriate affinity and selectivity. A variety of platforms based on emerging technologies have been discussed, and many have shown high sensitivity and low detection limits. However, validation of these methodologies is warranted before they are implemented in the food safety and regulatory field. Several obstacles associated with interference in real-sample analysis, the stability of these nanomaterials, and the reproducibility of assays remain to be solved before use of these methods for histamine testing. While significant progress has been made, an ideal, fast, and easy-to-use method for histamine detection remains elusive.

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REFERENCES

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AUTHOR INFORMATION

Corresponding Author

*V.A.: e-mail, [email protected]; tel, +420-545133350. ORCID

Vojtech Adam: 0000-0002-8527-286X Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Financial support from the Internal Grant Agency of the Faculty of Agronomy, Mendel University in Brno, no. AF-IGAIP-2018/076, ERDF “Multidisciplinary research to increase application potential of nanomaterials in agricultural practice” (No. CZ.02.1.01/0.0/0.0/16_025/0007314), and CEITEC 2020 (LQ1601) from the Ministry of Education, Youth and Sports of the Czech Republic under the National Sustainability Programme II is highly acknowledged.

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ABBREVIATIONS IEC, ion exchange chromatography; GC, gas chromatography; TLC, thin layer chromatography; FIA, flow injection analysis; APCI-MS, single-quadrupole mass spectrometry; LC, liquid chromatography; HPLC, high-pressure liquid chromatography; 780


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