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Modified QuEChERS combined with UPLC-MS/MS to determine eight biogenic amines in Xinjiang smoked horsemeat sausages

Abstract

A modified QuEChERS method coupled with ultra-high-performance liquid chromatography-tandem mass spectrometry (UPLC-MS/MS) was established for the simultaneous determination of eight biogenic amines (BAs) in Xinjiang smoked horsemeat sausages. The conditions of UPLC-MS/MS, extraction solvent and QuEChERS purification were optimized. The internal standard method was used for quantitative analysis. Results showed that the eight BAs exhibited good linearity (1-200 μg/L, correlation coefficient > 0.99). The limits of detection and quantification were 5 μg/kg and 10 μg/kg, respectively. The accuracy was between 80.4% and 111.4%, and the precision was less than 10%. The established method was effectively used for the determination of eight BAs in forty Xinjiang smoked horsemeat sausages. Results showed that tyramine was the major amine, followed by cadaverine, putrescine and spermine. Total BAs content ranged from 26.5 mg/kg to 352.9 mg/kg, the contents of BAs in Xinjiang smoked horsemeat sausages may pose a potential health risk.

Keywords:
biogenic amines; modified QuEChERS; ultra-high-performance liquid chromatography-tandem mass spectrometry; Xinjiang smoked horsemeat sausages

1 Introduction

Biogenic amines (BA) is a kind of bioactive low molecular weight nitrogenous organic compounds which have been found in different kinds of foods such as aquatic products, meat products and fermented products (Hu et al., 2012Hu, Y., Huang, Z., Li, J., & Yang, H. (2012). Concentrations of biogenic amines in fish, squid and octopus and their changes during storage. Food Chemistry, 135(4), 2604-2611. http://dx.doi.org/10.1016/j.foodchem.2012.06.121. PMid:22980848.
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; Ikonić et al., 2013Ikonić, P., Tasić, T., Petrović, L., Škaljac, S., Jokanović, M., Mandić, A., & Ikonić, B. (2013). Proteolysis and biogenic amines formation during the ripening of Petrovská klobása, traditional dry-fermented sausage from Northern Serbia. Food Control, 30(1), 69-75. http://dx.doi.org/10.1016/j.foodcont.2012.06.021.
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; Ruiz-Capillas & Jimenez-Colmenero, 2004Ruiz-Capillas, C., & Jimenez-Colmenero, F. (2004). Biogenic amines in meat and meat products. Critical Reviews in Food Science and Nutrition, 44(7-8), 489-499. http://dx.doi.org/10.1080/10408690490489341. PMid:15969322.
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). BAs are mainly formed by amino acid decarboxylation via bacteria with specific decarboxylase activity (Alan & Yildiz, 2021Alan, Y., & Yildiz, N. (2021). Effects of Lactobacillus used as the starter culture on naturally fermented pickled cabbage. Food Science and Technology. In press. http://dx.doi.org/10.1590/fst.45020.
http://dx.doi.org/10.1590/fst.45020...
). However, some other physiological effects (hypotension, nausea, palpitations, rashes, dizziness, headaches, tachycardia, hypertension, cardiac and emesis) may also occur if high concentrations of BAs are consumed (Gong et al., 2014Gong, X., Qi, N., Wang, X., Lin, L., & Li, J. (2014). Ultra-performance convergence chromatography (UPC2) method for the analysis of biogenic amines in fermented foods. Food Chemistry, 162, 172-175. http://dx.doi.org/10.1016/j.foodchem.2014.04.063. PMid:24874373.
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). The determination of biogenic amines in food products has received considerable interests not only because of their toxicity but also their usage as indicators of the degree of freshness or spoilage of food (Vinci & Antonelli, 2002Vinci, G., & Antonelli, M. (2002). Biogenic amines: quality index of freshness in red and white meat. Food Control, 13(8), 519-524. http://dx.doi.org/10.1016/S0956-7135(02)00031-2.
http://dx.doi.org/10.1016/S0956-7135(02)...
). In view of the degree of freshness food and the potential harmful effects of BAs, the development of sensitive and routine methods for their analysis in food is of great importance.

QuEChERS is a quick, easy, cheap, effective, rugged, and safe sample pretreatment technology based on dispersive solid phase extraction, which has been widely applied in the pretreatment of relatively simple samples, such as vegetable, fruit, beverage and wine (Xing et al., 2021Xing, L. J., Wang, Y., Luo, R. F., Li, X. Y., & Zou, L. J. (2021). Determination of 31 pesticide residues in wolfberry by LC-MS/MS and dietary risk assessment of wolfberry consumption. Food Science and Technology. In press. http://dx.doi.org/10.1590/fst.61921.
http://dx.doi.org/10.1590/fst.61921...
). But for traditional fermented meat products, due to the high fat content and protein content, the direct application of QuEChERS pretreatment method was not very effective. Therefore, it was necessary to remove the fat and protein in the sample and combine with QuEChERS pretreatment method. In recent years, the determination of BAs mainly focused on the matrix of seafood (Kaufmann & Maden, 2018Kaufmann, A., & Maden, K. (2018). Easy and fast method for the determination of biogenic amines in fish and fish products with liquid chromatography coupled to orbitrap tandem mass spectrometry. Journal of AOAC International, 101(2), 336-341. http://dx.doi.org/10.5740/jaoacint.17-0407. PMid:29157330.
http://dx.doi.org/10.5740/jaoacint.17-04...
), meat (Motaghifar et al., 2021Motaghifar, A., Akbari-Adergani, B., Rokney, N., & Mottalebi, A. (2021). Evaluating red meat putrefaction in long term storage in freezing condition based on co-variation of major biogenic amines and Total Volatile Nitrogen. Food Science and Technology, 41(Suppl. 1), 123-128. http://dx.doi.org/10.1590/fst.08120.
http://dx.doi.org/10.1590/fst.08120...
; Sun et al., 2016Sun, X., Zhou, K., Gong, Y., Zhang, N., Yang, M., Qing, D., Li, Y., Lu, J., Li, J., Feng, C., Li, C., & Yang, Y. (2016). Determination of biogenic amines in Sichuan-Style spontaneously fermented sausages. Food Analytical Methods, 9(8), 2299-2307. http://dx.doi.org/10.1007/s12161-016-0417-6.
http://dx.doi.org/10.1007/s12161-016-041...
), dairy (Adımcılar et al., 2017Adımcılar, V., Öztekin, N., & Bedia Erim, F. (2017). A direct and sensitive analysis method for biogenic amines in dairy products by capillary electrophoresis coupled with contactless conductivity detection. Food Analytical Methods, 11(5), 1374-1379. http://dx.doi.org/10.1007/s12161-017-1122-9.
http://dx.doi.org/10.1007/s12161-017-112...
), wine (Manetta et al., 2016Manetta, A. C., Di Giuseppe, L., Tofalo, R., Martuscelli, M., Schirone, M., Giammarco, M., & Suzzi, G. (2016). Evaluation of biogenic amines in wine: Determination by an improved HPLC-PDA method. Food Control, 62, 351-356. http://dx.doi.org/10.1016/j.foodcont.2015.11.009.
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; Redruello et al., 2017Redruello, B., Ladero, V., del Rio, B., Fernández, M., Martin, M. C., & Alvarez, M. A. (2017). A UHPLC method for the simultaneous analysis of biogenic amines, amino acids and ammonium ions in beer. Food Chemistry, 217, 117-124. http://dx.doi.org/10.1016/j.foodchem.2016.08.040. PMid:27664616.
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), beverages (Jain et al., 2015Jain, A., Gupta, M., & Verma, K. K. (2015). Salting-out assisted liquid-liquid extraction for the determination of biogenic amines in fruit juices and alcoholic beverages after derivatization with 1-naphthylisothiocyanate and high performance liquid chromatography. Journal of Chromatography A, 1422, 60-72. http://dx.doi.org/10.1016/j.chroma.2015.10.036. PMid:26518497.
http://dx.doi.org/10.1016/j.chroma.2015....
; Preti et al., 2016Preti, R., Bernacchia, R., & Vinci, G. (2016). Chemometric evaluation of biogenic amines in commercial fruit juices. European Food Research and Technology, 242(12), 2031-2039. http://dx.doi.org/10.1007/s00217-016-2701-5.
http://dx.doi.org/10.1007/s00217-016-270...
), sufu (Guan et al., 2013Guan, R., Liu, Z., Zhang, J., Wei, Y., Wahab, S., Liu, D., & Ye, X. (2013). Investigation of biogenic amines in sufu (furu): A Chinese traditional fermented soybean food product. Food Control, 31(2), 345-352. http://dx.doi.org/10.1016/j.foodcont.2012.10.033.
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; Tang et al., 2011Tang, T., Qian, K., Shi, T., Wang, F., Li, J., Cao, Y., & Hu, Q. (2011). Monitoring the contents of biogenic amines in sufu by HPLC with SPE and pre-column derivatization. Food Control, 22(8), 1203-1208. http://dx.doi.org/10.1016/j.foodcont.2011.01.018.
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), soy (Shukla & Kim, 2016Shukla, S., & Kim, M. (2016). Determination of biogenic amines and total aflatoxins: Quality index of starter culture soy sauce samples. Food Science and Biotechnology, 25(4), 1221-1224. http://dx.doi.org/10.1007/s10068-016-0194-4. PMid:30263398.
http://dx.doi.org/10.1007/s10068-016-019...
) and so on. Various methods have been developed for the analysis of BAs in foods mentioned above, including thin-layer chromatography (TLC) (Lapa-Guimarães & Pickova, 2004Lapa-Guimarães, J., & Pickova, J. (2004). New solvent systems for thin-layer chromatographic determination of nine biogenic amines in fish and squid. Journal of Chromatography A, 1045(1-2), 223-232. http://dx.doi.org/10.1016/j.chroma.2004.06.014. PMid:15378899.
http://dx.doi.org/10.1016/j.chroma.2004....
), gas chromatography-mass spectrometry (GC-MS) (Almeida et al., 2012Almeida, C., Fernandes, J. O., & Cunha, S. C. (2012). A novel dispersive liquid-liquid microextraction (DLLME) gas chromatography-mass spectrometry (GC-MS) method for the determination of eighteen biogenic amines in beer. Food Control, 25(1), 380-388. http://dx.doi.org/10.1016/j.foodcont.2011.10.052.
http://dx.doi.org/10.1016/j.foodcont.201...
; Papageorgiou et al., 2018Papageorgiou, M., Lambropoulou, D., Morrison, C., Namieśnik, J., & Płotka-Wasylka, J. (2018). Direct solid phase microextraction combined with gas chromatography: mass spectrometry for the determination of biogenic amines in wine. Talanta, 183, 276-282. http://dx.doi.org/10.1016/j.talanta.2018.02.006. PMid:29567176.
http://dx.doi.org/10.1016/j.talanta.2018...
), high performance liquid chromatography(HPLC) (Liu et al., 2018Liu, S., Xu, J., Ma, C., & Guo, C. (2018). A comparative analysis of derivatization strategies for the determination of biogenic amines in sausage and cheese by HPLC. Food Chemistry, 266, 275-283. http://dx.doi.org/10.1016/j.foodchem.2018.06.001. PMid:30381186.
http://dx.doi.org/10.1016/j.foodchem.201...
), high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS) (Dong & Xiao, 2017Dong, H., & Xiao, K. (2017). Modified QuEChERS combined with ultra high performance liquid chromatography tandem mass spectrometry to determine seven biogenic amines in Chinese traditional condiment soy sauce. Food Chemistry, 229, 502-508. http://dx.doi.org/10.1016/j.foodchem.2017.02.120. PMid:28372208.
http://dx.doi.org/10.1016/j.foodchem.201...
; Molognoni et al., 2018Molognoni, L., Daguer, H., de Sá Ploêncio, L. A., & De Dea Lindner, J. (2018). A multi-purpose tool for food inspection: Simultaneous determination of various classes of preservatives and biogenic amines in meat and fish products by LC-MS. Talanta, 178, 1053-1066. http://dx.doi.org/10.1016/j.talanta.2017.08.081. PMid:29136796.
http://dx.doi.org/10.1016/j.talanta.2017...
), liquid chromatography/quadrupole time-of-flight mass spectrometry (LC-QTOF) (Jia et al., 2011Jia, S., Kang, Y. P., Park, J. H., Lee, J., & Kwon, S. W. (2011). Simultaneous determination of 23 amino acids and 7 biogenic amines in fermented food samples by liquid chromatography/quadrupole time-of-flight mass spectrometry. Journal of Chromatography A, 1218(51), 9174-9182. http://dx.doi.org/10.1016/j.chroma.2011.10.040. PMid:22074649.
http://dx.doi.org/10.1016/j.chroma.2011....
). Among these methods, the sample pretreatment process of the TLC, GC-MS and HPLC methods was relatively complicated, time-consuming, requisite derivatization and low sensitivity, and the UPLC-MS/MS method was obviously better than other methods in analysis time, selectivity and anti-interference ability.

Xinjiang smoked horsemeat sausages are one of the most famous Chinese traditional meat products. It has gained lots of acceptance and popularity over China for hundred years due to its unique qualities and excellent nutritional characteristics (Lu et al., 2015Lu, S., Ji, H., Wang, Q., Li, B., Li, K., Xu, C., & Jiang, C. (2015). The effects of starter cultures and plant extracts on the biogenic amine accumulation in traditional Chinese smoked horsemeat sausages. Food Control, 50, 869-875. http://dx.doi.org/10.1016/j.foodcont.2014.08.015.
http://dx.doi.org/10.1016/j.foodcont.201...
). The making process of Xinjiang smoked horsemeat sausage is to mix the horse meat pieces with sugar, salt and spices in a certain proportion, and poured into the horse casings,after smoking, natural fermentation for 28 days (environmental temperature between 18 °C and 10 °C), one obtains the mature smoked horsemeat sausage. In the process of fermentation, horsemeat will form a unique flavor by lipid oxidation, protein oxidation and other processes improve the quality of smoked horsemeat sausage. However amino acids in horsemeat can also form biogenic amines by decarboxylation reaction during fermentation. Therefore, it is of great significance to evaluate and analyze the biogenic amine contents of Xinjiang smoked horsemeat sausages.

The purpose of this research is to establish a modified QuEChERS purification method coupled with a UPLC-MS/MS method for the simultaneous determination of eight BAs in Xinjiang smoked horsemeat sausages by optimizing the extraction solvent and adsorbent of the QuEChERS procedure. This method is applied to evaluate and analyze the contents of biogenic amines in Xinjiang smoked horsemeat sausages.

2 Materials and methods

2.1 Chemicals, reagents and standards

n-hexane and acetonitrile were purchased from Merck (HPLC grade, Darmstadt, Germany). Octadecylsilane (C18) adsorbent, primary secondary amine (PSA, 40-63 mm, 6 nm) adsorbent, graphitized carbon black (GCB) adsorbent, anhydrous magnesium sulfate (MgSO4), sodium chloride (NaCl) and formic acid (FA) were all purchased from CNW Technologies GmbH (Düsseldorf, Germany). Ultra-pure water (> 18.2 MΩ) was obtained from a Milli-Q water purification system (Millipore Corp., USA).

Standards of tyramine (TYR), phenethylamine (PEA), putrescine (PUT), cadaverine(CAD), histamine (HIS), tryptamine (TRP), spermidine (SPD), spermine (SPM) and 1,7-diaminoheptane (internal standard) were all acquired from Dr.Ehrenstorfer GmbH (Augsburg, Germany). All biogenic amines standards were of high purity grade (> 98%). Each standard substance was prepared 100 µg/mL individual standard stock solution with the acetonitrile, and all individual standard stock solutions were kept in a refrigerator at -20 °C.

2.2 Samples

Forty Xinjiang smoked horsemeat sausage samples were obtained from the local retail markets and department stores in Xinjiang Region. The origins of production were Urumchi city,Yili city, Changji city, Shihezi city and Tacheng city. All samples are vacuum packed. The samples were carried to the laboratory and stored at -20 °C until analysis.

2.3 Sample preparation

2.00 g smoked horsemeat sausage sample was accurately weighed, and transferred into a 50 mL plastic centrifuge tube. Then 100 µL of the 1.0 mg/L 1, 7-diaminoheptane and 5 mL of 10% ammonia water (V/V) were orderly added into the tube, and the mixture was vortexed for 30 s (A MS3 basic vortex mixer, IKA GmbH, Germany). After that, 10 mL of acetonitrile and 2 g of sodium chloride were further added, and the mixture was vortexed for 1 min and subsequently centrifuged for 3 min at 5000 g (3-330K high speed freezing centrifuge, Sigma Laborzentrifugen GmbH, Germany).

2.5 mL of the extraction solution was moved to a 10 mL high speed plastic centrifuge tube which contains 100 mg C18 and 100 mg of PSA. The above mixture was vortexed for 1 min and centrifuged for 5 min at 10000 g. After that,1.0 mL of supernatant was transferred into another 10 mL glass colorimetric tube, then it was subsequently blow-dried by nitrogen gas in a 40 °Cwaterbath(Nitrogen evaporator, Organomation Co., USA). Finally, 1.0 mL of 10% acetonitrile-water (V/V, containing 0.1% formic acid) was used to redissolve it. The redissolved solution was then filtered through a 0.22 µm filter membrane (Nylon, Shanghai ANPEL Laboratory Technologies Inc, China) and transferred into a sample bottle for UPLC-MS/MS analysis (Waters XevoTM TQ-S tandem mass spectrometer, Waters Co., USA). With respect to the sample solutions contain target analytes beyond the linearity range, determinations were performed after appropriate dilution with 10% acetonitrile-water (V/V, containing 0.1% formic acid).

2.4 Method validation

The optimized analytical method was validated in terms of linearity, limits of detection (LODs), limits of quantitation (LOQs), accuracy and precision for eight BAs in Xinjiang smoked horsemeat sausages.

Fermented sausages generally contain a variety of biogenic amines according to previous reviews (Suzzi & Gardini, 2003Suzzi, G., & Gardini, F. (2003). Biogenic amines in dry fermented sausages: a review. International Journal of Food Microbiology, 88(1), 41-54. http://dx.doi.org/10.1016/S0168-1605(03)00080-1. PMid:14527784.
http://dx.doi.org/10.1016/S0168-1605(03)...
). A series of mixed standard working solutions (1, 2, 5, 10, 20, 50, 100, 200 µg/L), which all contained 10 µg/L of the internal standard 1, 7-diaminoheptane, were all determined under the optimized conditions. The linear equations of the calibration curves were obtained by plotting the concentrations of the eight BAs and the corresponding peak areas, and the correlation coefficients (R2 values) were calculated. The LODs and LOQs of the eight BAs were determined by serially diluting a mixed standard solution with 10% acetonitrile-water (V/V, containing 0.1% formic acid). The LODs were determined when the signal to noise ratio (SNR) was higher than or equal to 3, and the LOQs were taken when the SNR was higher than or equal to 10.

To evaluate the accuracy and precision of the method, mixed standard solution of eight BAs was added to Xinjiang smoked horsemeat sausages, including three different concentration levels, and the spiked samples were determined under the optimized pretreatment and instrument conditions. The spiked samples were determined continuously for 6 times and the RSDs of the eight BAs were calculated.

2.5 Analysis of the Xinjiang smoked horsemeat sausages

Xinjiang smoked horsemeat sausages (40 samples) were randomly collected from different region in Xinjiang, including Urumchi city (8 samples), Yili city (12 samples), Changji city (8 samples), Shihezi city (6 samples) and Tacheng city (6 samples). The collected smoked horsemeat sausage samples were homogenized at 10000 r/min for 1 min and stored at -20 °C. All prepared samples were pretreated according to section 2.3, which were determined under the optimal conditions of chromatography and mass spectrometry.

3 Results and discussion

3.1 Optimization of UPLC-MS/MS conditions

The MS condition of eight BAs and 1,7-heptyldiamine were optimized by flow injection analysis of standard at a concentration of 1 μg/mL. According to the chemical structure of BAs, eight BAs and 1,7-heptyldiamineare easy to form positive ions in the ion source. The cone voltage and collision energy were optimized to obtain the highest intensity of parent ions and daughter ions. The characteristic ion pairs, cone voltage and collision energy of eight BAs and 1,7-heptyldiamine were presented in Table 1.

Table 1
MS parameters of eight BAs and the internal standard.

The selection of chromatographic column and mobile phases has greatly influence on results of analysis. Firstly, the effects of BEH C18 chromatographic column (100 mm×2.1 mm, 1.7 µm) and BEH HILIC chromatographic column (100 mm × 2.1 mm, 1.7 µm) on resolution of eight BAs were evaluated. Secondly, in order to study the effect of ionization efficiency, the addition of formic acid in mobile phase were investigated, including water + acetonitrile, 0.1% FA water + acetonitrile, water + 0.1% FA acetonitrile and 0.1% FA water + 0.1% FA acetonitrile.

The results showed that C18 column presented much better selectivities for the BAs. The peak shapes of the BAs separated by the C18 column were much more symmetrical and had better separation than those separated by the HILIC column. The addition of formic acid to the mobile phase improves the retention and peak shape of the biogenic amine while making ionization more adequate. Therefore, the BEH C18 chromatographic column and acetonitrile+water mobile phase (containing 0.1% formic acid) is the best condition for the determination of BAs (Figure 1).

Figure 1
Total ion chromatograms of eight BAs and the internal standard (1, 7-heptyldiamine), the concentration is 20 ng/mL.

3.2 Optimization of the extraction solvent

BAs were organic bases widely found in fermented meat products. Since BAs mostly existed as ions at neutral and acidic conditions, the extraction solvent was adjusted to alkaline state (pH=12) by ammonia water, thus could keep these BAs in molecular state and make them easier to distribute in organic extractant. The selection of extraction solvents directly affects the extraction efficiency of biogenic amines in smoked horsemeat sausages. The paper used acetonitrile and ethyl acetate as extraction solvents to evaluate the extraction efficiency of the solvent by the experiment of adding BAs standard in smoked horse sausages. Recoveries were used to evaluate the extraction effect. Results were presented in Figure 2 and it could be clearly observed from Figure 2 that the overall extraction recoveries of acetonitrile were higher than those of ethyl acetate. Therefore, acetonitrile was finally selected as the extraction solvent, resulting in recoveries ranging from 82.7% for SPD to 103.4% for CAD.

Figure 2
Comparison of the extraction efficiencies of different solvents (Spiked 100 μg/kg, n=3).

3.3 Optimization of the QuEChERS purification

QuEChERS technology is widely applied in the detection and analysis field. Chang et al. (2018)Chang, C.-C., Kao, T.-H., Zhang, D., Wang, Z., Inbaraj, B. S., Hsu, K.-Y., & Chen, B. H. (2018). Application of QuEChERS coupled with HPLC-DAD-ESI-MS/MS for determination of heterocyclic amines in commercial meat products. Food Analytical Methods, 11(11), 3243-3256. http://dx.doi.org/10.1007/s12161-018-1302-2.
http://dx.doi.org/10.1007/s12161-018-130...
applied QuEChERS-based purification technology for the determination of heterocyclic amines in commercial meat products and favorable recoveries were obtained, indicating that QuEChERS technology is suitable for purifying target analytes in sausages. However GCB has noticeable adsorption to aromatic amine compounds (Dong & Xiao, 2017Dong, H., & Xiao, K. (2017). Modified QuEChERS combined with ultra high performance liquid chromatography tandem mass spectrometry to determine seven biogenic amines in Chinese traditional condiment soy sauce. Food Chemistry, 229, 502-508. http://dx.doi.org/10.1016/j.foodchem.2017.02.120. PMid:28372208.
http://dx.doi.org/10.1016/j.foodchem.201...
), the purification effects of C18 and PSA frequently-used adsorbents were compared with each other. Due to the high fat content in acetonitrile extract solution of smoked horse sausage samples, the fat in acetonitrile extract solution was firstly removed by hexane, and then the mixed standard solution of eight biological amines was added to the acetonitrile extract solution. 2 mL of the upper acetonitrile solution was accurately transferred into a 5-mL centrifuge tube pre-loaded with C18 and PSA. After that the extraction solutions were vortexed and centrifuged. Next, 1 mL of the supernatant was transferred to a glass centrifuge tube and dried under flowing nitrogen in a 40 °C water-bath. Subsequently, the residue was redissolved using 1.0 mL of 10% acetonitrile-water (with 0.1% FA, V/V) and filtered through a 0.22 µm organic filter membrane. Finally, the supernatant was determined by UPLC-MS/MS, and the recovery was calculated.

The QuEChERS method is to add the right amount of adsorbent directly to the extracting solution, adsorbs as many impurities as possible while retaining the target. Compared with the ordinary SPE method, this is fewer steps such as washing and elution, which is faster and simpler. PSA adsorbent can remove polar interferences such as organic acids, pigments and sugars. C18 adsorbent removed non-polar interferences such as fat and ester from the sample matrix. Therefore, in this study, modified QuEChERS method was adopted in purification, and anhydrous magnesium sulfate was used to remove water, while PSA and C18 mixed adsorbents were used to effectively remove interferences in the extract. The results were shown in Figure 3. When the dosage of C18 and PSA was 100 mg respectively, the recovery of biogenic amine was the best and the purification effect was the best. Because the amount of adsorbent was too small, impurities can’t be completely adsorbed, if the amount of adsorbent was too large, it will adsorb certain biological amines. The results are consistent with those reported in the literature.

Figure 3
Recoveries of eight BAs purified with different absorbent types and dosages (Spiked 100 μg/kg, n=3).

3.4 Method validation

Linearity, detectability of the method

In the linearity studies, all the standard working solutions were determined under the optimal conditions of chromatography and mass spectrometry. Taking the concentration as the X-axis, the peak area as the Y-axis, linear regression analysis was performed. The results shown in Table 2 indicate that favourable linearities were obtained in the corresponding concentration range of each BA, and the coefficients of determination (R2) were higher than 0.99.

Table 2
Liner range, linear equation, R2, LODs and LOQs of the eight BAs.

The LODs and LOQs of the method were calculated according to the validated experimental results. The results showed that the LODs were 5 μg/kg, and the LOQs were 10 μg/kg (Table 2). The LODs and LOQs of this method are higher than those of the HPLC methods reported (Herrero et al., 2016Herrero, A., Sanllorente, S., Reguera, C., Ortiz, M. C., & Sarabia, L. A. (2016). A new multiresponse optimization approach in combination with a D-Optimal experimental design for the determination of biogenic amines in fish by HPLC-FLD. Analytica Chimica Acta, 945, 31-38. http://dx.doi.org/10.1016/j.aca.2016.10.001. PMid:27968713.
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; Piasta et al., 2014Piasta, A. M., Jastrzębska, A., Krzemiński, M. P., Muzioł, T. M., & Szłyk, E. (2014). New procedure of selected biogenic amines determination in wine samples by HPLC. Analytica Chimica Acta, 834, 58-66. http://dx.doi.org/10.1016/j.aca.2014.05.028. PMid:24928246.
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), and are basically consistent with those of the LC-MS/MS methods reported (Sagratini et al., 2012Sagratini, G., Fernández-Franzón, M., De Berardinis, F., Font, G., Vittori, S., & Mañes, J. (2012). Simultaneous determination of eight underivatised biogenic amines in fish by solid phase extraction and liquid chromatography–tandem mass spectrometry. Food Chemistry, 132(1), 537-543. http://dx.doi.org/10.1016/j.foodchem.2011.10.054. PMid:26434328.
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; Sirocchi et al., 2014Sirocchi, V., Caprioli, G., Ricciutelli, M., Vittori, S., & Sagratini, G. (2014). Simultaneous determination of ten underivatized biogenic amines in meat by liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). Journal of Mass Spectrometry, 49(9), 819-825. http://dx.doi.org/10.1002/jms.3418. PMid:25230178.
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; Dong & Xiao, 2017Dong, H., & Xiao, K. (2017). Modified QuEChERS combined with ultra high performance liquid chromatography tandem mass spectrometry to determine seven biogenic amines in Chinese traditional condiment soy sauce. Food Chemistry, 229, 502-508. http://dx.doi.org/10.1016/j.foodchem.2017.02.120. PMid:28372208.
http://dx.doi.org/10.1016/j.foodchem.201...
; Nalazek-Rudnicka & Wasik, 2017Nalazek-Rudnicka, K., & Wasik, A. (2017). Development and validation of an LC–MS/MS method for the determination of biogenic amines in wines and beers. Monatshefte für Chemie, 148(9), 1685-1696. http://dx.doi.org/10.1007/s00706-017-1992-y. PMid:28824206.
http://dx.doi.org/10.1007/s00706-017-199...
).

Accuracyand precision

The accuracy and precision were evaluated though which determined for each BA recoveries and RSDs at three different spiked concentrations in Xinjiang smoked horsemeat sausages. The results were shown in Table 3. The average recoveries ranged from 80.4% to 111.4% and RSDs were less than 10.0%. Indicating the accuracy and precision of the determination were satisfactory for eight BAs in Xinjiang smoked horsemeat sausages. The results are acceptable, which also comply with the AOAC criteria.

Table 3
Average recovery and RSD of the eight BAs in Xinjiang smoked horsemeat sausages (n=6).

3.5 Analysis of the Xinjiang smoked horsemeat sausages

The concentration of BAs in smoked horsemeat sausages in different regions of Xinjiang is shown in Table 4, and the average content of each region is shown in Figure 4. It can be seen from Table 4 that the BAs content of most samples is considerable difference, and the content of various BAs in the same sample is also significantly different. At the same time, the table also shows that YL1, YL12, WS5, WS6, CJ7 and TC4 six samples have only PUT, SPD, SPM three kinds of biological amine detected, which is completely different from other samples. After investigation and analysis, the reason for this result is mainly because these six samples are vacuum-packed products after high temperature sterilization.

Table 4
Detection results of the Xinjiang smoked horsemeat sausage samples.
Figure 4
Average contents of eight BAs in five different regions.

Tyramine is the dominant biogenic amine in Xinjiang smoked horsemeat sausages, the tyramine content ranged from ND to 151.5 mg/kg, which had a mean value of 57.8 mg/kg. Figure 4 shows that the average content of tyramine in Changji region is higher than that in other regions. Tyramine has also been found in fermented sausages in Turkey, Spain, France, Italy and Belgium, with a content range of 0 ~ 510 mg/kg (Bozkurt & Erkmen, 2004Bozkurt, H., & Erkmen, O. (2004). Effects of temperature, humidity and additiveson the formation of biogenic amines in sucuk during ripeningand storage periods. Food Science & Technology International, 10(1), 21-28. http://dx.doi.org/10.1177/1082013204041992.
http://dx.doi.org/10.1177/10820132040419...
; Papavergou et al., 2012Papavergou, E. J., Savvaidis, I. N., & Ambrosiadis, I. A. (2012). Levels of biogenic amines in retail market fermented meat products. Food Chemistry, 135(4), 2750-2755. http://dx.doi.org/10.1016/j.foodchem.2012.07.049. PMid:22980868.
http://dx.doi.org/10.1016/j.foodchem.201...
; Suzzi & Gardini, 2003Suzzi, G., & Gardini, F. (2003). Biogenic amines in dry fermented sausages: a review. International Journal of Food Microbiology, 88(1), 41-54. http://dx.doi.org/10.1016/S0168-1605(03)00080-1. PMid:14527784.
http://dx.doi.org/10.1016/S0168-1605(03)...
; Ansorena et al., 2002Ansorena, D., Montel, M. C., Rokka, M., Talon, R., Eerola, S., Rizzo, A., Raemaekers, M., & Demeyer, D. (2002). Analysis of biogenic amines innorthern and southern European sausages and role of flora in amineproduction. Meat Science, 61(2), 141-147. http://dx.doi.org/10.1016/S0309-1740(01)00174-7. PMid:22064002.
http://dx.doi.org/10.1016/S0309-1740(01)...
). The acceptable levels of tyramine should be ranged from 100 mg/kg to 800 mg/kg. Based on the present results, 25% of the fermented sausages were higher than 100 mg/kg. Similar result was reported by Lu et al. (2010)Lu, S., Xu, X., Zhou, G., Zhu, Z., Meng, Y., & Sun, Y. (2010). Effect of starter cultures on microbial ecosystem and biogenic amines in fermented sausage. Food Control, 21(4), 444-449. http://dx.doi.org/10.1016/j.foodcont.2009.07.008.
http://dx.doi.org/10.1016/j.foodcont.200...
, who found that the mean value of tyramine was 151.56 mg/kg in traditional Chinese sausages, and the concentration of tyramine in 57.1% samples was higher than 100 mg/kg.

Cadaverine is the second most abundant biogenic amine followed by tyramine in Xinjiang smoked horsemeat sausages. Due to the complex interaction between processing parameters, fresh meat quality, and microbial flora, cadaverine content varies greatly in different regions of Xinjiang. In this study, the content of cadaverine in Xinjiang smoked horsemeat sausages ranged from ND to 136.1 mg/kg, with an average content of 38.9 mg/kg.

The only amines present at significant levels in fresh meat used for fermented sausage production are spermidine and spermine, and, to a lesser extent, putrescine (Hernandez-Jover et al., 1997Hernandez-Jover, T., Izquierdo-Pulido, M., Veciana-Nogue’s, M. T., Mariné-Font, A., & Vidal-Carou, M. C. (1997). Biogenic amine and polyamine contents in meat and meat products. Journal of Agricultural and Food Chemistry, 45(6), 2098-2102. http://dx.doi.org/10.1021/jf960790p.
http://dx.doi.org/10.1021/jf960790p...
). High concentrations of putrescine and the presence of other amines have been attributed to microbial growth and depend on meat freshness. Putrescine and spermine are important BAs in the natural fermentation of smoked horsemeat sausages. The content of putrescine ranges from 1.1 mg/kg to 70.2 mg/kg, with an average of 19.5 mg/kg, and the content of spermine ranges from 5.6 mg/kg to 39.1 mg/kg, with an average of 20.7 mg/kg. The average content of putrescine and spermine (<30 mg/kg) was less than that of tyramine and cadaverine.

From a toxicological point of view, histamine is the most important biogenic amine, which can cause urticaria, hypotension, headache, flushing, abdominal pain, chemical poisoning and other human health problems (Kaufmann & Maden, 2018Kaufmann, A., & Maden, K. (2018). Easy and fast method for the determination of biogenic amines in fish and fish products with liquid chromatography coupled to orbitrap tandem mass spectrometry. Journal of AOAC International, 101(2), 336-341. http://dx.doi.org/10.5740/jaoacint.17-0407. PMid:29157330.
http://dx.doi.org/10.5740/jaoacint.17-04...
). In this study, the content of histamine was low and ranged from ND to 10.1 mg/kg, with an average of 3.6 mg/kg. The low content histamine could be explained that low temperature conditions do not favor histamine formation. Also, indigenous microflora apparently prevented the development of specific strains of some Enterobacteriace species capable to decarboxylate histidine (Bover-Cid et al., 2001Bover-Cid, S., Izquierdo-Pulido, M., & Carmen Vidal-Carou, M. (2001). Changes in biogenic amine and polyamine contents in slightly fermented sausages manufactured with and without sugar. Meat Science, 57(2), 215-221. http://dx.doi.org/10.1016/S0309-1740(00)00096-6. PMid:22061366.
http://dx.doi.org/10.1016/S0309-1740(00)...
).

Tryptamine, phenylethylamine and spermine were relatively low in Xinjiang smoked horsemeat sausages, and could be viewed as minor amines happening in fermented sausage. Tryptamine content ranged from ND to 15.6 mg/kg, with an average of 1.7 mg/kg. The content of phenylethylamine ranged from ND to 6.4 mg/kg, with an average of 1.5 mg/kg. The content of spermidine ranged from 0.6 mg/kg to 5.3 mg/kg, with an average of 2.7 mg/kg. This is similar to the results reported by Lu et al. (2010)Lu, S., Xu, X., Zhou, G., Zhu, Z., Meng, Y., & Sun, Y. (2010). Effect of starter cultures on microbial ecosystem and biogenic amines in fermented sausage. Food Control, 21(4), 444-449. http://dx.doi.org/10.1016/j.foodcont.2009.07.008.
http://dx.doi.org/10.1016/j.foodcont.200...
that tryptamine content in traditional Chinese sausage samples ranged from 0 to 28.2 mg/kg with an average of 7.24 mg/kg, and spermine content ranged from 0.1 mg/kg to 85.32 mg/kg with an average of 14.1 mg/kg. Gençcelep et al. (2008)Gençcelep, H., Kaban, G., Aksu, M. İ., Öz, F., & Kaya, M. (2008). Determination of biogenic amines in sucuk. Food Control, 19(9), 868-872. http://dx.doi.org/10.1016/j.foodcont.2007.08.013.
http://dx.doi.org/10.1016/j.foodcont.200...
also found similar results, with spermidine concentrations ranging from 0 to 10.7 mg/kg.

No standards or guidelines exist for the allowable concentrations of biogenic amines in fermented sausages. Determination of the exact toxicity threshold of biogenic amines in individuals is extremely difficult, since the toxic dose is strongly dependent on the efficiency of the detoxification mechanisms of each individual. Moreover, it must be noted that smaller amounts of biogenic amines may cause poisoning. Handling of raw materials and production technology for Xinjiang smoked horsemeat sausages are relatively primitive. These results indicate that the natural fermentation process used for Xinjiang smoked horsemeat sausages can result in the accumulation of high biogenic amines levels. Different environmental conditions and regions have some effect on biogenic amines content.

4 Conclusions

Xinjiang smoked horsemeat sausage is a kind of self-fermentation sausage, easy to produce various BAs. Up to now, the determination of BAs in fermented sausages mainly focused on HPLC method, because the determination of BAs by HPLC method is complicated and requires derivatization derivative process. So an easy, fast and effective method that can simultaneously measure eight BAs in Xinjiang smoked horsemeat sausage samples using a modified QuEChERS method and UPLC-MS/MS was established. Under optimized conditions of chromatography and mass spectrometry, Xinjiang smoked horsemeat sausage samples were extracted by acetonitrile and purified with 100 mg C18 adsorbent and 100 mg PSA adsorbent. This method had good selectivity, accuracy and precision using internal standard for quantification. The LODs and LOQs of the method were 5 μg/kg and 10 μg/kg, respectively. This method was successfully applied for the determination of eight BAs in forty Xinjiang smoked horsemeat sausage samples. The results showed that the tyramine was the major biogenic amines, followed by cadaverine, putrescine and spermine, which have a mean value of 57.8 mg/kg (ranging from ND to 151.5 mg/kg), 38.9 mg/kg (ranging from ND to 136.1 mg/kg), 19.5 mg/kg (ranging from 1.1 mg/kg to 70.2 mg/kg) and 20.7 mg/kg (ranging from 5.6 mg/kg to 35.7 mg/kg), respectively. TRY, PEA, HIS and SPD content were less than 20 mg/kg. Total biogenic amines content ranged from 26.5 mg/kg to 352.9 mg/kg in Xinjiang smoked horsemeat sausages. On the one hand, the presence of these amines has been related to the low quality of raw materials in which high proliferation of microorganisms occurs. On the other hand, the same raw material can lead to very different amine levels in final products depending on the presence of decarboxylating microorganisms, either derived from environmental contamination or from starter cultures, and the conditions supporting the growth and activity of amine-producing bacteria. Xinjiang smoked horsemeat sausages may pose a potential health risk. Therefore, it must be developed methods for preventing formation of biogenic amines that aim at eliminating the decarboxylating microbes in Xinjiang smoked horsemeat sausages, the use of high-quality raw materials, amine negative starter cultures and processing conditions which favour growth of the starter strains.

Acknowledgements

The authors wish to thank the anonymous reviewers, whose insightful comments and helpful suggestions significantly contributed to improving this paper.

  • Practical Application: Xinjiang smoked horsemeat sausages are one of the most famous Chinese traditional meat products. It has gained lots of acceptance and popularity over China for hundred years due to its unique qualities and excellent nutritional characteristics. However amino acids in horsemeat can also form biogenic amines by decarboxylation reaction during fermentation. The purpose of this research is to establish a modified QuEChERS purification method coupled with a UPLC-MS/MS method for the simultaneous determination of eight BAs in Xinjiang smoked horsemeat sausages by optimizing the extraction solvent and adsorbent of the QuEChERS procedure. This method is applied to evaluate and analyze the contents of biogenic amines in Xinjiang smoked horsemeat sausages.
  • #The author contributed to the work equally and should be regarded as co-first author.
  • Funding

    This research was funded by Major Project of National Agricultural Product Quality and Safety Risk Assessment, grant number GJFP2019020.

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Publication Dates

  • Publication in this collection
    11 Mar 2022
  • Date of issue
    2022

History

  • Received
    10 Oct 2021
  • Accepted
    18 Nov 2021
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