ANALYTICAL BIOCHEMISTRY

Analytical Biochemistry 346 (2005) 320326 www.elsevier.com/locate/yabio

Simple and rapid determination of histamine in food using a new histamine dehydrogenase from Rhizobium sp.
Tsuneo Sato , Tatsuo Horiuchi, Ikuko Nishimura
Research and Development Division, Kikkoman Corporation, Noda City, Chiba 278-0037, Japan Received 25 March 2005 Available online 26 September 2005

Abstract A colorimetric enzyme assay for the quantitative analysis of histamine in food has been developed using a new histamine dehydrogenase (HDH) from Rhizobium sp. The HDH speciWcally catalyzes the oxidation of histamine but not other biogenic amines such as putrescine and cadaverine. The principle of our photometric assay is as follows. The HDH catalyzes the oxidative deamination of histamine in the presence of 1-methoxy PMS (electron carrier), which converts WST-8 (tetrazolium salt) to a formazan. This product is measured in the visible range at 460 nm. The correlation between the histamine level and absorbance was acceptable, ranging from 0 to 96 M with histamine standard solutions, corresponding to 0 to 30 M of the reaction solution (r D 1.000, CV D 1.0% or less). Assays of canned tuna (in oil and soup) and raw tuna with 45675 mol/kg histamine added showed good recoveries of 96113, 98 108, and 100106%. The histamine contents of a commercial canned tuna and Wsh meal containing histamine at high concentrations were determined using the new method and other reference methods (HPLC method, Association of OYcial Analytical Chemists oYcial method, and two commercial enzyme immunoassay test kits). This simple and rapid enzymatic method is as reliable as the conventional methods. 2005 Elsevier Inc. All rights reserved.
Keywords: Histamine; Histamine dehydrogenase; Fish; Enzymatic method

The consumption of foods containing a large amount of histamine (a biogenic amine) has been implicated in causing allergy-like food poisoning known as scombroid poisoning [14]. Symptoms of Xushing and nettle rash appear on the face from 30 min to 1 h after the meal, followed by headache, diarrhea, and throbbing. Scombroid Wsh, including sardine, tuna, and mackerel, contain high concentrations of free histidine [47], which under certain conditions is decarboxylated by bacteria to produce high levels of histamine [8,9]. In addition, a large amount of histamine has been detected in fermented foods such as cheese, wine, and Wsh sauce [7,1015]. It is thought that histidine becomes histamine during fermentation in
*

Corresponding author. Fax: +81 4 7123 5550. E-mail address: 8901@mail.kikkoman.co.jp (T. Sato).

response to the decarboxylation action of lactic acid bacteria [16,17]. Allergy-like food poisoning generally occurs when food containing 1000 ppm (9000 mol/kg) or more of histamine is consumed [1]. However, poisoning may be caused in some individuals even when histamine has not reached this level. It has been reported that this is due to the synergistic action of amines other than histamine contained in food, such as putrescine and cadaverine [1820], but the mechanism of food-based histamine allergies has not yet been determined. In the United States, the toxic level that poses a risk to health is set at 500 ppm (4500 mol/kg), and the caution level is 50 ppm (450 mol/ kg). The European Union has also set a level of 100 200 ppm (9001800 mol/kg) for seafood, and Codex has also proposed regulations at this level [2123].

0003-2697/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.ab.2005.09.005

New histamine dehydrogenase from Rhizobium sp. / T. Sato et al. / Anal. Biochem. 346 (2005) 320326

321

An Association of OYcial Analytical Chemists (AOAC)1 oYcial method of analysis based on Xuorescent measurement has been established [6,24] and is recognized as the most suitable method for the determination of histamine contained in Wsh and fermented food. The method uses o-phthalaldehyde as a Xuorescent reagent, which yields a Xuorophore, and the intensity of the Xuorophore is measured by a photoXuorometer. However, to obtain derivatives from this Xuorophore and histamine, impurities in the sample must be removed. Thus, the labor and time required to carry out cleanup procedures are unavoidable. High-performance liquid chromatography (HPLC) and liquid chromatography are suitable methods of histamine analyses [1015,2529]. In addition to histamine, biogenic amines, such as putrescine and cadaverine, can be simultaneously and quantitatively determined by HPLC, but HPLC analyses are timeconsuming and an advanced operating technique is required. Recently, commercial enzyme immunoassays (EIAs) have become available [3032]. However, these kits are expensive. Moreover, a calibration curve must be determined for each measurement, for which roughly Wve measurements are required. Histamine assays based on enzyme method using histamine oxidase [5,3338] or histamine dehydrogenase (HDH) [39] are simple to perform and have recently been suggested to permit rapid measurement. However, these histamine oxidase and HDH also react with putrescine and tyramine [33 45]. Because these amines may be present in food at the same level as histamine [1,10,14,23,26,29], it is diYcult to selectively detect histamine by using above histamine oxidase and HDH. We recently found a new HDH from Rhizobium sp. 49 that acts more speciWcally on histamine than does the histamine-degrading bacterial enzyme mentioned previously. Using this enzyme, we developed a colorimetric enzyme method that can quantitatively determine histamine that is simpler, more rapid, and more economical than the conventional histamine assay methods. The sensitivity of the current procedure is equivalent to that of conventional methods for the detection of histamine in seafood. The current method provides a histamine assay that is easier to perform than previous methods, can be performed in a short time period, and permits the determination of multiple samples without expensive equipment or extensive technical skills. Materials and methods Chemicals All reagents were of analytical grade or of the highest grade available. Histamine dihydrochloride, putrescine
1 Abbreviations used: AOAC, Association of OYcial Analytical Chemists; HPLC, high-performance liquid chromatography; EIA, enzyme immunoassay; HDH, histamine dehydrogenase; DEAE, diethyl aminoethyl; 1-methoxy PMS, 1-methoxy-5-methylphenazinium methylsulfate; WST-8, 2-(2-methoxy-4-nitrophenyl)-3-(4-nitorophenyl)-5-(2,4-disulfophenyl)-2Htetrazolium monosodium salt; EDTA, ethylenediamine tetraacetic acid; DDBJ, DNA Data Bank of Japan; CV, coeYcient of variation.

dihydrochloride, cadaverine dihydrochloride, tyramine hydrochloride, tryptamine hydrochloride, spermidine trihydrochloride, spermine tetrahydrochloride, and agmatine sulfate salt were obtained form SigmaAldrich (Japan). Glucose, K2HPO4, KH2PO4, agar, (NH4)2SO4, and glycine for producing HDH were obtained from Wako Pure Chemical (Japan). Isolation and identiWcation of HDH-producing microorganisms Microorganisms with potent HDH were obtained from soil samples collected from several locations in Japan. Soil (1 g) was added to 10 ml of histamine broth (glucose 0.1% [w/ v], yeast extract [0.2%, w/v, Difco, USA], histamine dihydrochloride [0.1%, w/v], and K2HPO4 [0.05%, w/v] in tap water at, pH 6.75) and cultivated at 30 C for 1 week. Then, 0.1 ml of the culture was spread onto histamine agar plates (2% agar in histamine broth) and incubated at 30 C for 1 week. Approximately, 500 colonies on the culture plates were transferred to 10 ml of histamine broth and cultured at 30 C for 4 days. The cells were then collected by centrifugation at 18,000g for 10 min, suspended in 1 ml of 20 mM potassium phosphate buVer (pH 8.0), and sonicated. The homogenate was centrifuged at 18,000g for 10 min to remove intact cells and sonicated cell debris. The activities of histamine oxidase and HDH in the supernatant were then determined according to the method of Shimizu and coworkers [42]. IdentiWcation of isolated strain 49 was based on its 16S rDNA sequences, phylogenetic analysis, and morphological and physiological tests [46,47]. PuriWcation of HDH Strain 49 was grown aerobically at 30 C for 48 h in 20 L of histamine medium. Washed microorganisms were then suspended in 20 mM potassium phosphate buVer (pH 8.0) and sonicated. The homogenate was centrifuged at 18,000g for 30 min to remove intact cells and cell debris. Then (NH4)2SO4 was added to the above supernatant to 40% saturation and the precipitate formed was pelleted by centrifugation at 18,000g for 10 min. The supernatant to which (NH4)2SO4 was added to 60% saturation was centrifuged at 18,000g for 10 min, and the resultant precipitate was dissolved in 20 mM potassium phosphate buVer (pH 8.0) containing 13% (w/v) ammonium sulfate and dialyzed. The dialyzed enzyme solution was applied to a Toyopearl-Butyl650 (Tosoh, Japan) column equilibrated with the same buVer, and the absorbed protein was eluted with a linear (NH4)2SO4 gradient (130%). The active fractions were then pooled and subjected to ultraWltration such that the (NH4)2SO4 was exchanged for 20 mM potassium phosphate buVer (pH 8.0). The semipuriWed preparation was then applied to a DEAE Sephacel (Amersham Pharmacia) column equilibrated with 20 mM potassium phosphate buVer (pH 8.0). The absorbed protein was Wnally eluted with a linear NaCl gradient (0 1.0 M) in 20 mM potassium phosphate buVer (pH 8.0).

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New histamine dehydrogenase from Rhizobium sp. / T. Sato et al. / Anal. Biochem. 346 (2005) 320326

HDH activity assay An assay mixture (2.9 ml) of 83 mM glycineNaOH (pH 9.0), 0.32 mM histamine dihydrochloride (neutralized to, pH 7.0, with NaOH), 10 M 1-methoxy-5-methylphenazinium methylsulfate (1-methoxy PMS, electron carrier, Dojindo, Japan), and 100 M 2-(2-methoxy-4-nitrophenyl)-3-(4-nitrophenyl)-5-(2,4-disulfophenyl)-2H-tetra zolium monosodium salt (WST-8, Dojindo) was preincubated at 37 C for 5 min. The HDH sample was diluted with 50 mM glycineNaOH buVer (pH 9.0), and 0.1 ml of the sample was added to the assay mixture. The increase in absorbance in the mixture was measured at 460 nm. One unit of enzyme activity is deWned as the amount of enzyme that produces 1 mol imidazole acetaldehyde/min under the above assay conditions. An extinction coeYcient of 36 cm2/ mol was used for the calculation. Determination of protein and ammonia The protein concentration was determined using a modiWed Lowry method with a DC Protein Assay Kit (Bio-Rad, USA) with bovine plasma -globulin as the standard protein. The amount of ammonia was determined with an Ammonia Test Wako Kit (Wako). Enzymatic assay of histamine The principle of this method is shown in Fig. 1. Histamine is speciWcally decomposed by adding HDH in the presence of 1-methoxy PMS, which is an electron carrier. The tetrazolium salt (WST-8) develops color due to the electron transfer, and the histamine concentration is computed by measuring the increase in absorbance at 460 nm. The assay mixture (1.8 ml) consisted of 170 mM TrisHCl buVer (pH 9.0), 3.4 M 1-methoxy PMS, and 86 M WST-8. Sample (1.0 ml) containing histamine was added, and the mixture was preincubated at 37 C for 5 min. The colorimetric reaction was started by the addition of 0.4 ml of HDH solution (0.23 U/ml) diluted with 50 mM potassium phosphate buVer (pH 8.0). It was then incubated at 37 C for 5 min, after which the absorbance was measured at 460 nm. A blank contained distilled water instead of the enzyme solution.

Calculations Concentrations of histamine were estimated by the use of appropriate calibration curves. Linear regression (least squares method) was used for statistical analysis. Sample preparation Histamine was extracted from canned tuna and Wsh meal according to the following method. Approximately, 10 g of the sample was weighed and homogenized, and 1 g of the homogenized sample was transferred to a heat-resistant test tube with a cap. Exactly 24 ml of distilled water was added to the tube. The raw tuna sample was processed as above except that 24 ml of 0.1 M ethylenediamine tetraacetic acid (EDTA)2Na solution (pH 8.0) was added instead of distilled water. This procedure resulted in the samples being diluted 25-fold. They were subsequently boiled for 20 min and then cooled on ice. The supernatant was collected by Wltering through folded Wlter paper or centrifugation (10,000g for 5 min), and this supernatant was then used in the enzymatic histamine assay. Histamine assay by HPLC, AOAC, and EIA methods The HPLC method was carried out by the procedure of Kinoshita and Saito [25]. The AOAC method was performed using a Xuorometric assay oYcially recognized by AOAC International [24]. For the histamine assay by EIA methods, two commercial EIA test kitsHistamarine (Immunotech, France) and Veratox (Neogen, USA)were adopted. Results and discussion PuriWcation of HDH from Rhizobium sp. 49 Soil bacteria containing enzymes that reacted speciWcally with histamine were searched for in Japan, and 500 strains of bacteria were selected. Of the 500 strains, 499 had a histamine oxidase and one (strain 49) had an HDH. It was found that a crude extract of strain 49 did not act on amines contained in food, such as cadaverine, putrescine, and tyramine, but rather acted speciWcally on histamine. Therefore, we decided to use this strain for future research. When a system analysis was performed based on the physicochemical properties and the 16S rDNA base sequence of strain 49 (DNA Data Bank of Japan Accession No. AB21769), this bacterium was found to belong to the Rhizobium group and was named Rhizobium sp. 49. Rhizobium sp. 49 was cultured and HDH was puriWed by the method described in Materials and methods, the results of which are shown in Table 1. From 20 L of HDH culture medium, 0.00297 U/ml with a total activity of 59.4 U was obtained. HDH was puriWed 194-fold with a recovery of 40%. The preparation yielded a single band in SDS PAGE (data not shown).

Histamine dehydrogenase (HDH) Histamine 1-methoxy PMS WST- 8 formazan (at 460nm)

Imidazole acetaldehyde

1-methoxy PMS (reduced form)

WST- 8

Fig. 1. Principle of the new method for histamine assay using puriWed HDH.

New histamine dehydrogenase from Rhizobium sp. / T. Sato et al. / Anal. Biochem. 346 (2005) 320326 Table 1 Summary of HDH puriWcation from Rhizobium sp. 49

323

1.2
Yield (%) 100 103 73 40

(0.3)

Absorbance (460 nm)

Total activity (U) Crude extract Ammonium sulfate (60% sat.) Toyopearl-Butyl-650 DEAESephacel 59.4 61.2 43.4 23.8

Total protein (mg) 1800 548 34.0 3.71

SpeciWc activity (u/mg) 0.0330 0.112 1.28 6.40

1.0 0.8 0.6 0.4

Y= 0.0118X + 0.0127 r = 1.000

(0.5)

(0.6)

(0.9)

0.2 0.0

(0.5) (1.0)

(CV : %)

Properties of HDH from Rhizobium sp. 49 We found that HDH catalyzed the oxidation of histamine to imidazole acetaldehyde and ammonia when 1methoxy PMS was coupled to WST-8 (data not shown). HDH did not require an electron acceptor such as NAD+ or NADP+. The Km value and turnover number (kcat) of this enzyme were found to be 1.0 105 M and 8.3 s1, respectively, and the molecular mass was estimated at 150 kDa (dimer of 70 kDa) by SDSPAGE and gel Wltration by HPLC. The optimum pH was found to be between 9.0 and 11.5, and the enzyme was most active between 65 and 70 C. The enzyme was almost completely stable at 60 C for 15 min. To investigate the substrate speciWcity of HDH, an enzyme assay was performed using biogenic amines that are prominent in food. The puriWed enzyme exhibited no activity toward cadaverine, putrescine, tyramine, tryptamine, spermine, or spermidine. Only agmatine was slightly oxidized at a rate 10% that of histamine. The HDH of Nocardioides simplex IFO 12069 acts on putrescine at 30% the rate exhibited with histamine [48], and the histamine oxidase of Arthrobacter crystallopoietes KAIT-B-007 acts on tyramine at 36% the rate exhibited with histamine [37,44]. Putrescine and tyramine are often present in food at the same level as is histamine [1,10,14,23,26,29]. Thus, if these enzymes were used to analyze histamine in food, it would be diYcult to selectively quantitate histamine with them. Therefore, we suggest that the HDH derived from Rhizobium sp.49 is more suitable than other histaminedegrading bacterial enzymes for the analysis of histamine. Development of a histamine assay using puriWed HDH The linearity of the assay was determined using diVerent concentrations of histamine according to the method described in Materials and methods. Color development was achieved within 5 min. The same tendency was observed for every histamine concentration. As shown in Fig. 2, a linear relationship (r D 1) was found between histamine concentration and absorbance over a range from 0 to 96 M. The detection limit (blank + 3 SD) for the assay was 0.48 M in the histamine standard solution corresponding to 0.15 M reaction solution.

20

40

60

80

100

Histamine concentration (M)

Fig. 2. Linearity of the new histamine assay at various histamine concentrations. A plot of the absorbance at 460 nm against the histamine concentration (0, 4.8, 9.6, 24.0, 48.0, 72.0, and 96.0 M) of each sample solution (n D 16) is shown.

The within-day CV values (n D 16) for the histamine concentrations of 4.8, 9.6, 24.0, 48.0, 72.0, and 96.0 M in histamine standard solution corresponding to 1.5, 3.0, 7.5, 15.0, 23.0, and 30.0 M reaction solution were 1.0, 0.5, 0.9, 0.6, 0.5, and 0.3%, respectively. The between-day CV values (n D 16) were 2.5, 2.3, 2.3, 1.7, 1.0, and 1.9%, respectively. Because the calibration curve is excellent in terms of linearity and precision, we presumed that the histamine in a biological sample can be determined with good precision from the absorbance for only one given histamine standard solution. This means that our method has an advantage over the EIA method because the calibration curve by the EIA method is nonlinear and Wve histamine standards must be analyzed simultaneously. Also, a complex procedure is required to produce the nonlinear calibration curve. Because our enzymatic method is markedly better from a cost perspective and complex calibration curves are not required, it should be possible to adapt the procedure to a commercial kit. Recovery of spiked samples Histamine was added to the canned tuna (in oil or soup), which contained hardly any histamine, to give concentrations of 45, 90, 180, 450, and 675 mol/kg. The test solution was prepared by heat extraction with water using the method described in Materials and methods. The histamine in this test solution was then measured with the enzyme method. Good recovery (canned tuna in oil: 104.5 8.5%; canned tuna in soup: 103.0 5.0%) was obtained (Table 2). However, the recovery of histamine from raw Wsh by heat extraction with water was poor. Because histamine forms stable complexes with transition metal ions that exist in proteins or membranes of Wsh meat [49], it is necessary to use denaturing conditions to extract the histamine from Wsh meat. Boiling water extraction after autoclaving might make it possible to extract the histamine suYciently from raw Wsh, but this

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New histamine dehydrogenase from Rhizobium sp. / T. Sato et al. / Anal. Biochem. 346 (2005) 320326 Table 3 Comparison of the new assay and other reference methods for the evaluation of histamine in canned tuna Canned tunaa( mol/kg)b Raw tuna 48 95 180 458 698 100106 New assay HPLC method AOAC method EIA method 1c EIA method 2d
a b c d

Table 2 Recovery of histamine added to canned tuna (in oil and soup) and raw tuna Added histamine ( mol/kg) Recovered ( mol/kg)a Canned tuna in oil 45 102 194 459 648 96113 Canned tuna in soup 45 97 191 445 661 98108

45 90 180 450 675 Recovered %

a

4830 5090 4770 4170 5160

Average of three determinations.

Commercial canned tuna containing high levels of histamine. Average of three determinations. Histamarine: commercial EIA test kit. Veratox: commercial EIA test kit.

procedure is not practical. Because the chelate stability constants of the EDTAmetal ion complexes are higher than those of the histaminemetal ion complexes, the addition of EDTA will release histamine from the metal ion as the EDTA binds to it. Therefore, we expected that boiling in a solution containing EDTA would make it possible to recover histamine as eYciently as the method that uses boiling water extraction after autoclaving. In practice, we found that heat extraction using 0.1 M EDTA (pH 8.0) was suitable in the case of a raw Wsh sample, and good recovery (103.0 3.0%) was obtained (Table 2). In summary, heat treatment with water or with EDTA solutions was suYcient to extract histamine quantitatively from canned tuna and raw tuna. As mentioned above for the HPLC method and the AOAC method, strong acids or methanol are often used for the extraction of a sample [5 7,1014,26,28,50] and caution is required in handling these reagents. Moreover, cleanup with ion exchange resins is also required. Our method has the additional advantage that extraction can be easily performed in a short time period. Analysis of biological samples In a commercial canned tuna sample where a high concentration of histamine was detected, the amount of histamine in this sample was measured using our method, the HPLC method, the AOAC method, and the EIA methods (commercial kits: Histamarine, Veratox). As shown in Table 3, the results using the current procedure were equivalent to those using the other methods. Then the amount of histamine in Wve Wsh meal samples was analyzed with our enzymatic method, HPLC method, and EIA method (Table 4). As in the case of the canned tuna, a good correlation between this method and the other methods was observed. From these results, we found that our method was able to quantitate histamine in food in approximately 1 h by means of a series of simple operations. The new procedure was validated against conventional methods. Thus, our method is suitable for the analysis of foods where histamine toxicity is a concern.

Table 4 Evaluation of histamine in Wsh meal feed for Wsh and poultry Sample number 1 New assay ( mol/kg) HPLC method EIA method 1a 10,800 11,300 12,900 2 1970 1745 2230 3 5670 5500 4570 4 1740 2020 1710 5 1060 1310 1120

Note. Average of three determinations. a Veratox: commercial EIA test kit.

Conclusions A new enzymatic method for the measurement of histamine in seafood has been developed. A high correlation was observed between the results obtained by this method and those obtained by conventional methods. Our enzymatic method has many advantages; extraction is simple, a histamine calibration curve can be easily drawn, and the histamine amount can be rapidly measured. This method would be a useful tool for assessing food spoilage and preventing scombroid poisoning. Acknowledgments We thank T. Fujii, M. Suzuki, N. Yamaji, Y. Imai, and M. Bakke for their valuable discussions. References
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