Development and Application of Quartz Crystal Microbalance Sensor

May 13, 2014 - To rapidly detect histamine (HA) in foods, a novel material for HA-specific recognition was synthesized by a sol–gel process and coat...
0 downloads 0 Views 2MB Size
Download PDF
Article pubs.acs.org/JAFC

Development and Application of Quartz Crystal Microbalance Sensor Based on Novel Molecularly Imprinted Sol−Gel Polymer for Rapid Detection of Histamine in Foods Jie Dai, Yan Zhang, Mingfei Pan, Lingjie Kong, and Shuo Wang* Key Laboratory of Food Nutrition and Safety, Ministry of Education of China, Tianjin University of Science and Technology, Tianjin 300457, China ABSTRACT: To rapidly detect histamine (HA) in foods, a novel material for HA-specific recognition was synthesized by a sol− gel process and coated on a quartz crystal microbalance (QCM) sensor. The Scatchard model was used to evaluate the adsorption performance of the material; high affinity for HA was demonstrated. Based on QCM frequency change, the sensor exhibited linear behavior for HA concentrations of 0.11 × 10−2 to 4.45 × 10−2 mg L−1, a detection limit of 7.49 × 10−4 mg kg−1 (S/N = 3), high selectivity for HA (selectivity coefficient >4) compared with structural analogues, good reproducibility, and longterm stability. The sensor was used to determine the concentration of HA in spiked fish products; the recovery values were satisfactory (93.2−100.4%) and compared well with those obtained by high-performance liquid chromatography (correlation coefficient, r2 = 0.9965). KEYWORDS: histamine, quartz crystal microbalance sensor, sol−gel, molecularly imprinted polymer

■

recognition layer to the surface of the quartz crystal.13 Recently, molecularly imprinted polymers (MIPs) have been used as recognition elements in membranes fabricated on the surfaces of quartz crystals.14,15 Molecular imprinting mimics natural molecular recognition16−18 by forming nanocavities that are complementary to a template molecule in shape, size, and functional groups upon removal of the template from the synthesized organic polymer. As a result, MIPs are able to recognize a specific target molecule. A QCM sensor for HA based on a MIP synthesized via bulk polymerization has been developed,19 but it exhibited a low resonance frequency of 34.09 Hz at 100 μM. Traditional bulk polymerization of MIPs is of limited application because grinding of the bulk polymer will damage the imprinted sites.20 Compared with those prepared by bulk polymerization, MIPs synthesized using a sol−gel process show higher specificity for their template molecule,21 and also exhibit faster mass transfer and binding kinetics.22 Sol−gel-based imprinted polymers that incorporate the template molecule into a rigid inorganic network are easy to prepare and possess good chemical stability.23,24 In the present research, we synthesize a new molecularly imprinted material for HA-specific recognition by a sol−gel process. A quartz crystal is covered with the developed material to produce a novel HA-MIP QCM sensor for HA with high selectivity and sensitivity. The equilibrium parameters and selectivity of the developed QCM sensor are investigated, and its ability to detect HA in food samples is examined.

INTRODUCTION Histamine (HA), although a common biogenic amine, has been considered an important cause of an allergy-like food poisoning for many years. Food poisoning induced by HA results from enzymatic decarboxylation of histidine (HIS) in numerous foods, such as scombroid and some nonscombroid fish when stored improperly.1 The processes of cooking, freezing, or smoking will not destroy HA once it has formed.2 Consuming excess HA can lead to adverse health effects including headaches, nausea, diarrhea, rashes, and even death.3 To reduce the incidence of HA poisoning associated with fish consumption, the United States Food and Drug Administration recommend that fish should be chilled immediately upon death and a maximum HA level of 50 ppm in fish for consumption.4 Chromatography techniques, including high-performance liquid chromatography (HPLC), thin-layer chromatography, and gas chromatography,5−8 and immunological assays9 are typical methods for HA determination. However, these methods are highly technical, cumbersome, and timeconsuming. Especially in HPLC, pre- or postcolumn derivation is required to enhance the low ultraviolet (UV) absorbance of aliphatic amines,10 prolonging the analytical process. In addition, chromatographic equipment is not portable, making it unsuitable for field analysis. Although they possess the advantage of high throughput, immunological assays are easily affected by environmental factors. Piezoelectric quartz crystal microbalance (QCM) sensors offer a timely alternative for HA detection because of their simplicity, ease of miniaturization, and precise quantitative analysis.11 A QCM used as a transducer of a sensor can measure nanogram-order changes in mass loading on the quartz crystal surface by observation of the frequency shift based on the Sauerbrey equation.12 This approach is promising not only because of the advantages mentioned above but also because selective sensing can be achieved by adding an appropriate © 2014 American Chemical Society

Received: Revised: Accepted: Published: 5269

March 4, 2014 May 9, 2014 May 13, 2014 May 13, 2014 dx.doi.org/10.1021/jf501092u | J. Agric. Food Chem. 2014, 62, 5269−5274

Journal of Agricultural and Food Chemistry

■

Article

where C is the initial concentration of analyte in solution (mg L−1), Q is the adsorption capacity at adsorption equilibrium (mg·g−1), Kd is the equilibrium disassociation constant at the binding site (mg L−1), and Qmax is the saturated adsorption capacity (mg·g−1).25−27 The NIP was also tested using the above procedure. Mean adsorption values obtained from triplicate measurements of MIP and NIP were determined and compared. Modification of a Quartz Crystal Surface with HA-MIP. Before modification, the quartz crystal electrode surface was cleaned in piranha solution (30% H2O2:98% H2SO4; 1:3 v/v) for 2 min to remove possible residual chemicals, and thoroughly rinsed with deionized water. HA-MIP or NIP (48.50 mg) was suspended in PVCDCM (0.7 wt % solution). After ultrasonication to obtain a homogeneous solution, 5.0 μL of the mixture was carefully dispensed onto the immobilized quartz crystal surface. The modified quartz crystal was dried (30 min, 25 °C) and stored at room temperature in a vacuum chamber before use. Figure 1 outlines the processes of HAMIP sensor construction and adsorption.

MATERIALS AND METHODS

Reagents, Materials, and Apparatus. HA, HIS, tyramine (TYR), phenylethylamine (PEA), 3-mercaptopropyltriethoxysilane (MPTES), and tetraethoxysilane (TEOS) were supplied by SigmaAldrich (St. Louis, MO, USA). Polyvinyl chloride (PVC, Mw = 8000) and dichloromethane (DCM) were obtained from Alfa Aesar (Tianjin, China). Methanol, acetonitrile, NaH2PO4, Na2HPO4, and other reagents were purchased from Tianjin No. 1 Chemical Reagent Factory (Tianjin, China). All chemicals were analytical reagent grade. Cans of sardines, mackerel, saury, tuna, salmon, and Spanish mackerel for sample analysis were purchased from a local market. Phosphate-buffered saline (PBS; pH 7.6) was prepared by mixing 0.2 M NaH2PO4 with 0.2 M Na2HPO4 (1:4 v/v). Frequency change (Δf, Hz) was recorded using a QCM (QCM922, Princeton Applied Research, Princeton, NJ, USA) equipped with a quartz crystal resonator (AT-cut, 9 MHz, platinum electrode (0.196 cm2, 100 Å), Princeton Applied Research) and Teflon holder (Princeton Applied Research). The quartz crystal was positioned in the Teflon holder to ensure that only one side of the Pt electrode was in contact with the solution. The holder was placed vertically in a static detection cell to minimize any gravity-induced precipitation on the crystal surface. A magnetic stirrer (HJ-6A, Jin Tan Sheng Lan Instrument Co., Jiang Su, China) was used throughout the experiments to ensure homogeneous and complete interaction between agents. UV spectrophotometer (Cary 50-Bio, Varian, Palo Alto, CA, USA) was used to evaluate the ability of the MIP to adsorb the analyte. The morphology of the modified quartz crystals was investigated by scanning electron microscopy (SEM, SU1510, Hitachi, Tokyo, Japan). An HPLC analyzer (LC-10ATVP, Shimadzu, Kyoto, Japan) was used to validate the results obtained for real samples using the HA-MIP QCM sensor. Sol−Gel Synthesis of HA-MIP. A novel HA-imprinted polymer was synthesized through hydrolytic cross-linking of silanol groups using a sol−gel process as follows: HA (0.10 g) was dissolved in methanol (5.0 mL) and mixed with MPTES (0.5 mL) in a 25 mL round-bottomed flask. After 30 min, TEOS (1.09 mL) and 0.1 M NH3·H2O (0.5 mL) were added and the mixture was incubated at 55 °C in a water bath for 12 h. The product was filtered and then aged in a vacuum oven at 60 °C for 10 h. After protonation in a mixture of CH3OH and 1.0 M HCl (4:1 v/v, 100 mL) for 4 h, the solid product was collected by vacuum filtration and rinsed with deionized distilled water until the eluent reached neutral pH. Then, the product was dried in a vacuum oven at 60 °C until constant weight was obtained. The original template was removed by Soxhlet extraction in a mixture of methanol and acetic acid (9:1 v/v, 300 mL) until no HA was detected by UV absorbance measurement at 210 nm. The obtained polymer was dried in a vacuum oven at 60 °C and stored hermetically until further use. All solutions were mixed by gentle magnetic stirring to ensure homogeneous distribution and complete interaction between agents. Nonimprinted polymer (NIP) was also prepared in a manner identical to that used to synthesize MIP, except that the template was omitted. Adsorption of HA-MIP. HA-MIP (20.0 mg) was mixed with PBS (5.0 mL, pH = 7.6) containing different concentrations of HA (10, 20, 30, 40, 60, 80, 100, and 120 mg L−1) in polypropylene centrifuge tubes. After vigorous shaking at 150 rpm for 2 h and centrifugation at 4500g for 10 min, the amount of unbound HA in each supernatant was determined by UV absorbance measurement at 210 nm. The adsorption capacity (Q, mg·g−1) of HA-MIP was calculated as follows:

Q = (C i − Cf ) × V /W

Figure 1. HA-MIP sensor construction and adsorption. QCM Sensor Detection. After anchoring of the prepared quartz crystal into the Teflon holder, the assembled HA-MIP QCM sensor was immersed in PBS (20.0 mL) at room temperature. A steady resonant frequency ( f 0, Δf < 1.0 Hz) was obtained after equilibration for 5 min. A small aliquot of analyte solution was injected into the solution. After equilibration for 5 min, a stable frequency change caused by analyte binding was obtained and recorded. After each test, the MIP-modified quartz crystal was washed with 0.1 M HCl and deionized water until the frequency recovered to f 0 and the crystal could be reused. Throughout the entire testing process, the solution was stirred at 240 rpm to accelerate the transmission of analyte. Analyses were performed in triplicate, and the average value of the obtained frequency shift (Δf, Hz) was used to calculate the mass of HA adsorbed onto the crystal surface according to the Sauerbrey equation:28

Δf = − 2.26 × 10−6Δmf0 2 /A

where f 0 is the original frequency of the quartz crystal (Hz), Δm is the mass change (g), and A is the surface area of the electrode (cm2). For comparison, the NIP-modified QCM sensor was also tested using the same procedure. Sample Preparation for HA-MIP QCM Sensor Analysis. Sample slurry (1.0 g) was mixed with HClO4 (10.0 mL, 0.4 M) to induce protein precipitation. After homogenization for 15 min, the mixture was centrifuged. The collected supernatant was extracted with n-hexane (2:1 v/v) for further fat separation; the n-hexane supernatant was discarded. The defatting procedure was repeated twice, and then the product was dried using a rotary evaporator at 45 °C. The residue was redissolved in PBS (20.0 mL, pH = 7.6) and analyzed using the HA-MIP QCM sensor. For the recovery test, slurries of sardine, mackerel, or saury were spiked with HA at 25, 100, and 400 μg kg−1; the procedure used to extract HA was the same as that described above. Sample Pretreatment for HPLC Analysis. HPLC was used to confirm the accuracy of the developed sensor. The procedure up until rotary evaporation was the same as described above; the residue was then reconstituted with HClO4 (4.0 mL, 0.4 M) and derivatized as described in previous literature29 with slight modification. The

(1)

where Ci and Cf are the initial and final concentration of analyte in solution, respectively (mg L−1), V is the volume of solution (L), and W is the mass of polymer (g). Scatchard analysis of binding isotherms was used to evaluate the binding capacity of HA-MIP for the template. The relevant equation is

Q /C = (− Q + Q max )/Kd

(3)

(2) 5270

dx.doi.org/10.1021/jf501092u | J. Agric. Food Chem. 2014, 62, 5269−5274

Journal of Agricultural and Food Chemistry

Article

redissolved solution (1.0 mL) was placed in a 5 mL brown volumetric flask. NaOH (200 μL, 2.0 M), saturated NaHCO3 (300 μL), and dansyl chloride (4.0 mL, 0.02 M) were added in succession. After incubation at 60 °C for 30 min, NH3·H2O solution (100.0 μL, 25 wt %) was added to remove excess dansyl chloride. Each solution was adjusted to 5.0 mL with acetonitrile and filtered through a 0.22 μm filter before HPLC analysis. HPLC Analysis. In HPLC analysis, an analytical octadecylsilyl-3 column (4.6 × 250 mm, 5 μm particle size, Shimadzu) was used with acetonitrile:water (65:35 v/v) as the mobile phase at a flow rate of 1.0 mL min−1. The injection volume and detection wavelength were 20 μL and 254 nm, respectively. All spectral and chromatographic data were obtained and processed using Class-VP software.

in the selective recognition of HA by the MIP. The nonlinearity of the Scatchard model plot for the NIP (Figure 2B) was caused by the disordered arrangement of recognition sites in the NIP system resulting from the lack of template during the polymerization process. The lower adsorption of HA by the NIP compared with that by the MIP could be attributed to the lack of specific binding sites within the polymer matrix. Optimization of the PVC:HA-MIP Ratio. In this experiment, PVC was chosen as the matrix material to immobilize the prepared HA-MIP particles on the quartz crystal, because the recognition sites of a MIP encapsulated in PVC are easily accessible to the template30 and the solubility of PVC in DCM could enhance the processability of the insoluble MIP.31 The PVC:HA-MIP ratio used to modify the quartz crystal surface affected the capability of the prepared HA-MIP QCM sensor. Although more PVC could enhance the attachment of MIP particles, the amount of MIP immobilized on the surface of the quartz crystal was decreased, reducing the sensitivity and specificity of the modified sensor. Therefore, to ensure maximum and steady adsorption of HA on the quartz crystal surface, the amount of MIP used should be as large as possible while still effective adhering to the crystal. In this work, frequency changes (Δf) of HA-MIP QCM sensors prepared using PVC-DCM solutions (0.7 wt %) containing various ratios of PVC to MIP (PVC:MIP = 1:1, 1:2, 1:3, 1:4, 1:5, and 1:6 m/ m) were compared at the same HA concentration (4.45 × 10−2 mg L−1). Δf increased with the ratio of PVC to MIP until it reached 1:5. Adding further MIP (1:6) caused Δf to decrease sharply. Based on these results, a ratio of PVC to MIP of 1:5 was chosen for modification of the QCM sensor. Morphological Characterization. SEM was used to evaluate the morphology of the HA-MIP-modified quartz crystal surface (Figure 3). Figure 3A shows that the layer containing MIP was completely adhered to the transducer surface, with a relatively uniform dispersion of polymer particles. Compared with the bare electrode (Figure 3B), the modified one possessed a much rougher surface, which provided a larger surface area for the specific adsorption of the target molecule. Influence of Test Solution pH on QCM Detection. In the process of HA recognition, the HA-MIP QCM sensor selectively recognizes HA through the acid−base interaction between the immobilized −SH groups of the sensor and −NH2 group of HA; the latter is affected by the adsorption microenvironment, particularly pH. Therefore, it is necessary to optimize the pH of the test solution so that the analyte readily adsorbs onto the prepared sensor. HA solutions (4.45 × 10−2 mg L−1) with different pH ranging from 6.0 to 8.8 were prepared in PBS for frequency analysis. Δf increased slowly for pH 6.0−6.8, before reaching a peak at pH 7.6; it then decreased continuously as the solution pH value increased beyond 7.6. This phenomenon might be attributed to the competition between the abundant H+ and −SH to react with −NH2 of HA under acidic conditions. The interaction between HA and MPTES would be decreased by the abundance of OH− groups when the pH exceeded 7.6. Therefore, the optimum pH of the test solution was 7.6, which was used in further tests to guarantee excellent recognition ability of the developed QCM sensor. Evaluation of Binding Performance. The frequency responses of the MIP and NIP QCM sensors for HA were compared in solutions with HA concentrations ranging from 0.11 × 10−2 to 6.67 × 10−2 mg L−1 to evaluate their specific

■

RESULTS AND DISCUSSION Adsorption of HA-MIP. The abilities of the prepared MIP and reference NIP to adsorb HA were evaluated in PBS (pH = 7.6) containing different concentrations of HA. The adsorption isotherms of the polymers were obtained and assessed by Scatchard analysis (Figure 2). As shown in Figure 2A, with

Figure 2. (A) Binding isotherms and (B) Scatchard plots of MIP and NIP for HA.

increasing HA concentration, the adsorption capacities (Q, mg· g−1) of both the MIP and NIP increased. At an HA concentration of 120 mg L−1, Q of MIP (8.28 mg·g−1) was 5.2 times that of NIP (1.60 mg·g−1), indicating that MIP has a markedly greater ability than NIP to adsorb HA. The Scatchard plot in Figure 2B reveals that a good linear relationship between Q/C and Q (mg·g−1) was obtained of Q/C = −0.0057Q + 0.1169, with a correlation coefficient of 0.9964. Kd and Qmax calculated using this model were 175.44 mg L−1 and 20.51 mg·g−1, respectively, suggesting that the MIP has a high affinity for HA. These results also demonstrate that recognition sites or cavities (presumably based on the acid−base pair resulting from the reaction between −NH2 of HA and −SH of MPTES) form in the MIP; these would play an important role 5271

dx.doi.org/10.1021/jf501092u | J. Agric. Food Chem. 2014, 62, 5269−5274

Journal of Agricultural and Food Chemistry

Article

Good linearity of the relationship of frequency change with concentration was obtained for HA concentrations from 0.11 × 10−2 to 4.45 × 10−2 mg L−1 (correlation coefficient = 0.9978). The calculated detection limit (S/N = 3) of the MIP QCM sensor for HA was 7.49 × 10−4 mg kg−1, which is lower than that for HA by HPLC (0.054 mg kg−1).6 A PVC-modified QCM sensor did not show any detectable frequency response to HA at selected concentrations, indicating that PVC used to immobilize the MIP on the electrode surface did not affect the specific recognition of HA by the proposed sensor. Kinetic and Selectivity Experiments. The adsorption kinetics of the developed sensor were tested in PBS containing HA (4.45 × 10−2 mg L−1, pH = 7.6) under continuous stirring. A steady frequency response (−206.1 Hz) was obtained within 10 min, indicating that the HA-MIP QCM sensor could achieve adsorption equilibrium in a short period, which would be helpful for rapid detection of HA. The selectivity (or specificity) of the prepared QCM sensor is another important parameter to evaluate. For this purpose, different concentrations (0.11 × 10−2 to 4.45 × 10−2 mg L−1) of TYR, HIS, and PEA (Figure 5A), which are structurally

Figure 3. SEM images of the surface of a quartz crystal (A) before and (B) after HA-MIP modification.

adsorptive capability; the results are presented in Figure 4. Δf increased with HA concentration for both modified sensors. At

Figure 5. (A) Chemical structures of HA, HIS, TYR, and PEA. (B) Selectivity of the HA-MIP QCM sensor for different analytes.

similar to HA, in PBS (pH = 7.6) were tested with the HA-MIP QCM sensor. The selectivity coefficient (SC), defined as αHA/ αanalyte, where α is the slope of the analyte calibration curve, was used to assess the selectivity of the HA-MIP QCM sensor for HA. The detection results illustrated in Figure 5B reveal much weaker frequency responses for HIS, TYR, and PEA than for HA with SC of 4.18, 6.43, and 5.17, respectively, indicating that the developed sensor has excellent selectivity and specificity for HA. This selectivity results from the tuned cavities of the HAMIP that are complementary to HA in size, shape, and functional groups. Reproducibility and Stability. The reproducibility and stability of the developed QCM are important for successful HA detection. Therefore, the same HA-MIP QCM sensor was used to evaluate the frequency change in PBS containing HA (4.45 × 10−2 mg L−1, pH = 7.6) 7 times continuously. After each test, the imprinted sensor was washed with 0.1 M HCl and

Figure 4. Frequency responses of MIP and NIP QCM sensors in solutions containing different concentrations of HA.

any particular concentration, the HA-MIP QCM sensor showed a larger frequency response than the NIP one, demonstrating the differential binding capability of the MIP sensor for HA. At an HA concentration of 6.67 × 10−2 mg L−1, the frequency change for the MIP sensor was −229.0 Hz, about 5 times that of the NIP one (−45.0 Hz). This might be caused by imprinting the MIP with HA, which caused cavities that specifically fit HA in terms of spatial structure and functional groups to form during polymerization. The frequency response tended to equilibrate at HA concentrations above 6.67 × 10−2 mg L−1, because the MIP became saturated with adsorbed HA. The small response of the NIP-modified QCM sensor is attributed to nonspecific adsorption of HA. 5272

dx.doi.org/10.1021/jf501092u | J. Agric. Food Chem. 2014, 62, 5269−5274

Journal of Agricultural and Food Chemistry

Article

concentration of HA in six different samples (canned sardines, mackerel, saury, tuna, salmon, and Spanish mackerel) was determined by HPLC. The results of both methods were recorded, and the regression equation was calculated to be y = 1.0086x − 0.0214 with a correlation coefficient of 0.9965, signifying the accuracy of the HA-MIP QCM sensor. Compared with HPLC, the developed QCM sensor enhanced HA detection efficiency greatly because it is sensitive, easy to operate, stable for more than 6 months, and portable for field analysis, and it does not require pre- or postcolumn derivation. The results show that the MIP-based QCM sensor can be used for accurate HA detection in food samples.

deionized water sequentially until the resonance frequency reached its original value. The frequency change during repeated testing decreased slightly from 206.1 to 196.3 Hz; this loss of just 4.8% confirmed the good recyclability and stability of the MIP QCM sensor for HA detection. The stability of the HA-MIP QCM sensor over a long period of time was also demonstrated. After hermetic storage at room temperature for 6 months, the average frequency shift of the quartz crystal was 195.0 Hz, which is only 5.4% less than the initial frequency shift of 206.1 Hz. This result further confirms the excellent stability of the developed QCM sensor, which suggests that the MIP is also highly stable. Recovery Test. Samples of canned sardines, saury, and mackerel were spiked with HA at three levels (25, 100, and 400 μg kg−1). The HA concentration of each sample was detected 3 times under the same conditions. The relative standard deviation (RSD, %) of the repeated measurements was calculated to determine the precision of the method; the results are listed in Table 1. The overall precision ranged from

■

Corresponding Author

*Tel: +86 22 60601456. Fax: +86 22 60601332. E-mail: s. [email protected]. Funding

This work was supported by the Ministry of Science and Technology of the People’s Republic of China (Project No. 2011AA100807), China Postdoctoral Science Foundation (Project No. 2013M540210), and the Program for Changjiang Scholars and Innovative Research Team in University (IRT1166).

Table 1. Recoveries of HA from Spiked Food Samples Determined by the HA-MIP QCM Sensor (n = 3) orig concn (μg kg−1), mean ± SD

spiked concn (μg kg−1)

canned sardines

67.7 ± 0.1

canned saury

55.2 ± 0.5

25 100 400 25 100 400 25 100 400

sample

canned mackerel

102.7 ± 0.3

detected concn (μg kg−1), mean ± SD 92.8 167.1 446.8 79.8 148.4 429.3 127.9 200.8 494.6

± ± ± ± ± ± ± ± ±

1.9 2.5 2.6 3.5 2.1 1.1 1.1 1.4 3.5

RSD (%)

recovery (%)

2.0 1.5 0.6 4.4 1.4 0.3 0.9 0.7 0.7

100.4 99.4 94.8 98.4 93.2 93.5 100.2 99.1 98.4

Notes

The authors declare no competing financial interest.

■

Table 2. Content of HA in Samples Detected by the HA-MIP QCM Sensor and HPLC (n = 3) HA-MIP QCM sensor sample canned sardines canned tuna canned salmon canned mackerel canned Spanish mackerel canned saury

HPLC

RSD (%)

detected concn (μg kg−1), mean ± SD

RSD (%)

76.7 ± 1.5

2.0

67.7 ± 0.1

0.1

299.0 ± 1.6 669.4 ± 3.9

0.5 0.6

278.4 ± 0.5 666.3 ± 1.2

0.2 0.2

111.5 ± 1.7

1.5

102.7 ± 0.3

0.3

463.8 ± 2.5

0.5

427.6 ± 0.7

0.2

91.4 ± 2.6

2.8

55.2 ± 0.5

0.9

REFERENCES

(1) Hungerford, J. M. Scombroid poisoning: a review. Toxicon 2010, 56, 231−243. (2) Phuvasate, S.; Su, Y. C. Effects of electrolyzed oxidizing water and ice treatments on reducing histamine-producing bacteria on fish skin and food contact surface. Food Control 2010, 21, 286−291. (3) Švarc-Gajić, J.; Stojanović, Z. Determination of histamine in cheese by chronopotentiometry on a thin film mercury electrode. Food Chem. 2010, 124, 1172−1176. (4) Scombrotoxin (histamine) formation. In Fish and fisheries products hazards and controls guidance; Center for Food Safety and Applied Nutrition, Office of Seafood, Food and Drug Administration: Washington, DC, 2001; pp 83−102. (5) Jadidi-Niaragh, F.; Mirshafiey, A. Histamine and histamine receptors in pathogenesis and treatment of multiple sclerosis. Neuropharmacology 2010, 59, 180−189. (6) Tang, T.; Qian, K.; Shi, T. U.; Wang, F.; Li, J. Q.; Cao, Y. S.; Hu, Q. B. Monitoring the contents of biogenic amines in sufu by HPLC with SPE and pre-column derivatization. Food Control 2011, 22, 1203−1208. (7) Zhai, H. L.; Yang, X. Q.; Li, L. H.; Xia, G. B.; Cen, J. W.; Huang, H.; Hao, S. X. Biogenic amines in commercial fish and fish products sold in southern China. Food Control 2012, 25, 303−308. (8) Jia, S.; Kang, Y. P.; Park, J. H.; Lee, J.; Kwon, S. W. Determination of biogenic amines in Bokbunja (Rubus coreanus Miq.) wines using a novel ultra-performance liquid chromatography coupled with quadrupole-time of flight mass spectrometry. Food Chem. 2012, 132, 1185−1190. (9) Muscarella, M.; Lo Magro, S.; Campaniello, M.; Antonio, A.; Stacchini, P. Survey of histamine levels in fresh fish and fish products collected in Puglia (Italy) by ELISA and HPLC with fluorimetric detection. Food Control 2012, 31, 211−217. (10) Pérez, S.; Bartrolí, J.; Fàbregas, E. Amperometric biosensor for the determination of histamine in fish samples. Food Chem. 2013, 141, 4066−4072. (11) Ö zkütük, E. B.; Diltemiz, S. E.; Ö zalp, E.; Ö zalp, E.; Say, R.; Ersöz, A. Ligand exchange based paraoxon imprınted QCM sensor. Mater. Sci. Eng.: C 2012, 33, 938−942.

0.3 to 4.4%, and the recovery values were also good, ranging from 93.2 to 100.4%, suggesting that results obtained using the HA-MIP QCM sensor were both accurate and reproducible. Actual Sample Analysis. Using the established sample pretreatment method, the concentration of HA in six different samples (canned sardines, mackerel, saury, tuna, salmon, and Spanish mackerel) was measured by the HA-MIP QCM sensor. The results of these measurements are shown in Table 2. HPLC Validation. Traditional HPLC was used to validate the results obtained using the HA-MIP QCM sensor. The

detected concn (μg kg−1), mean ± SD

AUTHOR INFORMATION

5273

dx.doi.org/10.1021/jf501092u | J. Agric. Food Chem. 2014, 62, 5269−5274

Journal of Agricultural and Food Chemistry

Article

(12) Hauptmann, P. Resonant sensors and applications. Sens. Actuators, A 1991, 26, 371−377. (13) Escuderos, M. E.; Sánchez, S.; Jiménez, A. Virgin olive oil sensory evaluation by an artificial olfactory system, based on Quartz Crystal Microbalance (QCM) sensors. Sens. Actuators, B 2010, 147, 159−164. (14) Sener, G.; Ozgur, E.; Yılmaz, E.; Uzun, L.; Say, R.; Denizli, A. Quartz crystal microbalance based nanosensor for lysozyme detection with lysozyme imprinted nanoparticles. Biosens. Bioelectron. 2010, 26, 815−821. (15) Hussain, M.; Iqbal, N.; Lieberzeit, P. A. Acidic and basic polymers for molecularly imprinted folic acid sensors-QCM studies with thin films and nanoparticles. Sens. Actuators, B 2012, 176, 1090− 1095. (16) Vasapollo, G.; Sole, R. D.; Mergola, L.; Lazzoi, M. R.; Scardino, A.; Scorrano, S.; Mele, G. Molecularly imprinted polymers: present and future prospective. Int. J. Mol. Sci. 2011, 12, 5908−5945. (17) Zhang, H. Q.; Ye, L.; Mosbach, K. Non-covalent molecular imprinting with emphasis on its application in separation and drug development. J. Mol. Recognit. 2006, 19, 248−259. (18) Alexander, C.; Andersson, H. S.; Andersson, L. I.; Ansell, R. J.; Kirsch, N.; Nicholls, I. A.; O’Mahony, J.; Whitcombe, M. J. Molecular imprinting science and technology: a survey of the literature for the years up to and including 2003. J. Mol. Recognit. 2006, 19, 106−180. (19) Horemans, F.; Alenus, J.; Bongaers, E.; Weustenraed, A.; Thoelen, R.; Duchateau, J.; Lutsen, L.; Vanderzande, D.; Wagner, P.; Cleij, T. J. MIP-based sensor platforms for the detection of histamine in the nano-and micromolar range in aqueous media. Sens. Actuators, B 2010, 148, 392−398. (20) Tamayo, F. G.; Casillas, J. L.; Martin-Esteban, A. Highly selective fenuron-imprinted polymer with a homogeneous binding site distribution prepared by precipitation polymerisation and its application to the clean-up of fenuron in plant samples. Anal. Chim. Acta 2003, 482, 165−173. (21) Cummins, W.; Duggan, P.; McLoughlin, P. A comparative study of the potential of acrylic and sol−gel polymers for molecular imprinting. Anal. Chim. Acta 2005, 542, 52−60. (22) Fang, G. Z.; Tan, J.; Yan, X. P. An ion-imprinted functionalized silica gel sorbent prepared by a surface imprinting technique combined with a sol-gel process for selective solid-phase extraction of cadmium (II). Anal. Chem. 2005, 77, 1734−1739. (23) Olwill, A.; Hughes, H.; O’Riordain, M.; McLoughlin, P. The use of molecularly imprinted sol−gels in pharmaceutical separations. Biosens. Bioelectron. 2004, 20, 1045−1050. (24) Su, P. G.; Hung, F. C.; Lin, P. H. Fabrication, characterization and sensing properties of Cu (II) ion imprinted sol−gel thin film on QCM. Mater. Chem. Phys. 2012, 135, 130−136. (25) Mohajeri, S. A.; Ebrahimi, S. A. Preparation and characterization of a lamotrigine imprinted polymer and its application for drug assay in human serum. J. Sep. Sci. 2008, 31, 3595−3602. (26) Yin, X. Y.; Liu, Q. S.; Jiang, Y. F.; Luo, Y. M. Development of andrographolide molecularly imprinted polymer for solid-phase extraction. Spectrochim. Acta, Part A 2011, 79, 191−196. (27) Scatchard, G. The attractions of proteins for small molecules and ions. Ann. N.Y. Acad. Sci. 1949, 51, 660−672. (28) Sauerbrey, G. Verwendung von Schwingquarzen zur Wägung dünner Schichten und zur Mikrowägung. Z. Phys. 1959, 155, 206−222. (29) Mey, E. D.; Drabik-Markiewicz, G.; Maere, H. D.; Peeters, M.C.; Derdelinckx, G.; Paelinck, H.; Kowalska, T. Dabsyl derivatisation as an alternative for dansylation in the detection of biogenic amines in fermented meat products by reversed phase high performance liquid chromatography. Food Chem. 2012, 130, 1017−1023. (30) Chronakis, I. S.; Jakob, A.; Hagström, B.; Ye, L. Encapsulation and selective recognition of molecularly imprinted theophylline and 17β-estradiol nanoparticles within electrospun polymer nanofibers. Langmuir 2006, 22, 8960−8965. (31) Matsuguchi, M.; Uno, T. Molecular imprinting strategy for solvent molecules and its application for QCM-based VOC vapor sensing. Sens. Actuators, B 2006, 113, 94−99. 5274

dx.doi.org/10.1021/jf501092u | J. Agric. Food Chem. 2014, 62, 5269−5274