The application of biosensors in complex real-world samples is often complicated due to the combined effects and interferences of various compounds on the biosensor signal. However, thorough modelling and chemometric methods allow us to evaluate the impact of different analytes and calibrate these biosensors for the multiplexed analyses of the targeted compounds. A typical multianalyte mixture includes biogenic amines, produced during the putrefaction of proteins. Meanwhile, the detection of particular biogenic amines is a valuable tool for assessing the freshness and quality of a wide variety of protein-containing foods. In the current study, we analysed the signal of biosensors for the simultaneous detection of four major biogenic amines (cadaverine, putrescine, histamine, and spermidine) and proposed two different approaches for their multivariate calibration. The evaluation of the proposed models and the calculation of their characteristic coefficients were based on experimental data from over three hundred different mixtures with randomly varying substrate concentrations.
Albrecht-Ruiz, M., Clark-Leza, D. and Aleman-Polo, M. 1999. Rapid method for biogenic amines evaluation in fish meal. J. Aquat. Food Prod. Technol., 8(4), 71–83.
https://doi.org/10.1300/J030v08n04_07
Alonso-Lomillo, M. A., Domínguez-Renedo, O., Matos, P. and Arcos-Martínez, M. J. 2010. Disposable biosensors for determination of biogenic amines. Anal. Chim. Acta, 665(1), 26–31.
https://doi.org/10.1016/j.aca.2010.03.012
Baker, D. A. and Gough, D. A. 1996. Dynamic delay and maximal dynamic error in continuous biosensors. Anal. Chem., 68(8), 1292–1297.
https://doi.org/10.1021/ac960030d
Ben-Gigirey, B., Vieites Baptista De Sousa, J. M., Villa, T. G. and Barros-Velazquez, J. 1998. Changes in biogenic amines and microbiological analysis in albacore (Thunnus alalunga) muscle during frozen storage. J. Food Prot., 61(5), 608–615.
https://doi.org/10.4315/0362-028X-61.5.608
Bóka, B., Adányi, N., Virág, D., Sebela, M. and Kiss, A. 2012. Spoilage detection with biogenic amine biosensors, comparison of different enzyme electrodes. Electroanalysis, 24(1), 181–186.
https://doi.org/10.1002/elan.201100419
Bongaers, E., Alenus, J., Horemans, F., Weustenraed, A., Lutsen, L., Vanderzande, D. et al. 2010. A MIP-based biomimetic sensor for the impedimetric detection of histamine in different pH environments. Phys. Status Solidi (A) Appl. Mater. Sci., 207(4), 837–843.
https://doi.org/10.1002/pssa.200983307
Carelli, D., Centonze, D., Palermo, C., Quinto, M. and Rotunno, T. 2007. An interference free amperometric biosensor for the detection of biogenic amines in food products. Biosens. Bioelectron., 23(5), 640–647.
https://doi.org/10.1016/j.bios.2007.07.008
Carsol, M. A. and Mascini, M. 1999. Diamine oxidase and putrescine oxidase immobilized reactors in flow injection analysis: a comparison in substrate specificity. Talanta, 50(1), 141–148.
https://doi.org/10.1016/S0039-9140(99)00111-3
DeBeer, J., Bell, J. W., Nolte, F., Arcieri, J. and Correa, G. 2021. Histamine limits by country: a survey and review. J. Food Prot., 84(9), 1610–1628.
https://doi.org/10.4315/JFP-21-129
del Valle, M. 2010. Electronic tongues employing electrochemical sensors. Electroanalysis, 22(14), 1539–1555.
https://doi.org/10.1002/elan.201000013
Di Paolo, M. L., Lunelli, M., Fuxreiter, M., Rigo, A., Simon, I. and Scarpa, M. 2011. Active site residue involvement in monoamine or diamine oxidation catalysed by pea seedling amine oxidase. FEBS J., 278(8), 1232–1243.
https://doi.org/10.1111/j.1742-4658.2011.08044.x
Erdag, D., Merhan, O. and Yildiz, B. 2019. Biochemical and pharmacological properties of biogenic amines. In Biogenic Amines (Proestos, C., ed.). IntechOpen.
https://doi.org/10.5772/intechopen.81569
European Commission 2005. Commission Regulation (EC) No. 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. OJEU, L 338.
Gardini, F., Özogul, Y., Suzzi, G., Tabanelli, G. and Özogul, F. 2016. Technological factors affecting biogenic amine content in foods: a review. Front. Microbiol., 7.
https://doi.org/10.3389/fmicb.2016.01218
Getzinger, T. W. 1994. The costs and benefits of abstract interpretation-driven Prolog optimization. In Static Analysis. SAS 1994. Lecture Notes in Computer Science, 864 (Le Charlier, B., ed.). Springer, Berlin, Heidelberg.
https://doi.org/10.1007/3-540-58485-4_30
Halász, A., Baráth, Á., Simon-Sarkadi, L. and Holzapfel, W. 1994. Biogenic amines and their production by microorganisms in food. Trends Food Sci. Technol., 5(2), 42–49.
https://doi.org/10.1016/0924-2244(94)90070-1
Horemans, F., Alenus, J., Bongaers, E., Weustenraed, A., Thoelen, R., Duchateau, J. et al. 2010. MIP-based sensor platforms for the detection of histamine in the nano- and micromolar range in aqueous media. Sens. Actuators B: Chem., 148(2), 392–398.
https://doi.org/10.1016/j.snb.2010.05.003
Hosseini, S. V., Hamzeh, A., Moslemi, M., Lashkan, A. B., Iglesias, A. and Feás, X. 2013. Effect of delayed icing on biogenic amines formation and bacterial contribution of iced common carp (Cyprinus carpio). Molecules, 18(12), 15464–15473.
https://doi.org/10.3390/molecules181215464
Kivirand, K. and Rinken, T. 2007. Purification and properties of amine oxidase from pea seedlings. Proc. Estonian Acad. Sci. Chem., 56(4), 164–171.
https://doi.org/10.3176/chem.2007.4.01
Kivirand, K. and Rinken, T. 2009. Interference of the simultaneous presence of different biogenic amines on the response of an amine oxidase-based biosensor. Anal. Lett., 42(11), 1725–1733.
https://doi.org/10.1080/00032710902993860
Kivirand, K. and Rinken, T. 2011. Biosensors for biogenic amines: the present state of art mini-review. Anal. Lett., 44(17), 2821–2833.
https://doi.org/10.1080/00032719.2011.565445
Kivirand, K., Sõmerik, H., Oldekop, M.-L., Rebane, R. and Rinken, T. 2016. Effect of spermidine and its metabolites on the activity of pea seedlings diamine oxidase and the problems of biosensing of biogenic amines with this enzyme. Enzyme Microb. Technol., 82, 133–137.
https://doi.org/10.1016/j.enzmictec.2015.09.007
Křížek, M., Vácha, F., Vejsada, P. and Pelikánová, T. 2011. Formation of biogenic amines in fillets and minced flesh of three freshwater fish species stored at 3 °C and 15 °C. Acta Vet. Brno, 80(4), 365–372.
https://doi.org/10.2754/avb201180040365
Lange, J. and Wittmann, C. 2002. Enzyme sensor array for the determination of biogenic amines in food samples. Anal. Bioanal. Chem., 372, 276–283.
https://doi.org/10.1007/s00216-001-1130-9
Li, L., Wen, X., Wen, Z., Chen, S., Wang, L. and Wei, X. 2018. Evaluation of the biogenic amines formation and degradation abilities of Lactobacillus curvatusfrom Chinese bacon. Front. Microbiol., 9.
https://doi.org/10.3389/fmicb.2018.01015
Luque de Castro, M. D. and Herrera, M. C. 2002. Enzyme inhibition-based biosensors and biosensing systems: questionable analytical devices. Biosens. Bioelectron., 18(2–3), 279–294.
https://doi.org/10.1016/S0956-5663(02)00175-6
Martynko, E. and Kirsanov, D. 2020. Application of chemometrics in biosensing: a brief review. Biosensors, 10(8).
https://doi.org/10.3390/bios10080100
Mattsson, L., Xu, J., Preininger, C., Tse Sum Bui, B. and Haupt, K. 2018. Competitive fluorescent pseudo-immunoassay exploiting molecularly imprinted polymers for the detection of biogenic amines in fish matrix. Talanta, 181, 190–196.
https://doi.org/10.1016/j.talanta.2018.01.010
McGuirl, M. A. and Dooley, D. M. 1999. Copper-containing oxidases. Curr. Opin. Chem. Biol., 3(2), 138–144.
https://doi.org/10.1016/S1367-5931(99)80025-8
Medda, R., Padiglia, A. and Floris, G. 1995. Plant copper-amine oxidases. Phytochemistry, 39(1), 1–9.
https://doi.org/10.1016/0031-9422(94)00756-J
Mitsubayashi, K., Kubotera, Y., Yano, K., Hashimoto, Y., Kon, T., Nakakura, S. et al. 2004. Trimethylamine biosensor with flavin-containing monooxygenase type 3 (FMO3) for fish-freshness analysis. Sens. Actuators B: Chem., 103(1–2), 463–467.
https://doi.org/10.1016/j.snb.2004.05.006
Muñoz-Esparza, N. C., Latorre-Moratalla, M. L., Comas-Basté, O., Toro-Funes, N., Veciana-Nogués, M. T. and Vidal-Carou, M. C. 2019. Polyamines in food. Front. Nutr., 6.
https://doi.org/10.3389/fnut.2019.00108
Neofotistos, A.-D. G., Tsagkaris, A. S., Danezis, G. P. and Proestos, C. 2019. Emerging trends in biogenic amines analysis. In Biogenic Amines (Proestos, C., ed.). IntechOpen.
https://doi.org/10.5772/intechopen.81274
Niculescu, M., Nistor, C., Frébort, I., Peč, P., Mattiasson, B. and Csöregi, E. 2000. Redox hydrogel-based amperometric bienzyme electrodes for fish freshness monitoring. Anal. Chem., 72(7), 1591–1597.
https://doi.org/10.1021/ac990848
Önal, A. 2007. A review: current analytical methods for the determination of biogenic amines in foods. Food Chem., 103(4), 1475–1486.
https://doi.org/10.1016/j.foodchem.2006.08.028
Özogul, F., Gökbulut, C., Özogul, Y. and Özyurt, G. 2006. Biogenic amine production and nucleotide ratios in gutted wild sea bass (Dicentrarchus labrax) stored in ice, wrapped in aluminium foil and wrapped in cling film at 4°C. Food Chem., 98(1), 76–84.
https://doi.org/10.1016/j.foodchem.2005.04.037
Papageorgiou, M., Lambropoulou, D., Morrison, C., Kłodzińska, E., Namieśnik, J. and Płotka-Wasylka, J. 2018. Literature update of analytical methods for biogenic amines determination in food and beverages. Trends Anal. Chem., 98, 128–142.
https://doi.org/10.1016/j.trac.2017.11.001
Pietrangeli, P., Nocera, S., Mondovì, B. and Morpurgo, L. 2003. Is the catalytic mechanism of bacteria, plant, and mammal copper-TPQ amine oxidases identical? Biochim. Biophys. Acta - Proteins Proteom., 1647(1–2), 152–156.
https://doi.org/10.1016/S1570-9639(03)00083-9
Pietrangeli, P., Federico, R., Mondovì, B. and Morpurgo, L. 2007. Substrate specificity of copper-containing plant amine oxidases. J. Inorg. Biochem., 101(7), 997–1004.
https://doi.org/10.1016/j.jinorgbio.2007.03.014
Pospiskova, K., Safarik, I., Sebela, M. and Kuncova, G. 2013. Magnetic particles-based biosensor for biogenic amines using an optical oxygen sensor as a transducer. Microchim. Acta, 180, 311–318.
https://doi.org/10.1007/s00604-012-0932-0
Prabhakar, R. and Siegbahn, P. E. M. 2001. A theoretical study of the mechanism for the reductive half-reaction of pea seedling amine oxidase (PSAO). J. Phys. Chem. B, 105(19), 4400–4408.
https://doi.org/10.1021/jp003343s
Rinken, T. 2003. Determination of kinetic constants and enzyme activity from a biosensor transient signal. Anal. Lett., 36(8), 1535–1545.
https://doi.org/10.1081/AL-120021535
Rinken, T. and Tenno, T. 2001. Dynamic model of amperometric biosensors. Characterisation of glucose biosensor output. Biosens. Bioelectron., 16(1–2), 53–59.
https://doi.org/10.1016/S0956-5663(00)00133-0
Rinken, T., Rinken, P. and Kivirand, K. 2011. Signal analysis and calibration of biosensors for biogenic amines in the mixtures of several substrates. In Biosensors – Emerging Materials and Applications (Serra, P. A., ed.). IntechOpen.
https://doi.org/10.5772/16308
Ruiz-Capillas, C. and Moral, A. 2004. Free amino acids and biogenic amines in red and white muscle of tuna stored in controlled atmospheres. Amino Acids, 26(2), 125–132.
https://doi.org/10.1007/s00726-003-0054-4
Sánchez-Pérez, S., Comas-Basté, O., Costa-Catala, J., Iduriaga-Platero, I., Veciana-Nogués, M. T., Vidal-Carou, M. C. and Latorre-Moratalla, M. L. 2022. The rate of histamine degradation by diamine oxidase is compromised by other biogenic amines. Front. Nutr., 9.
https://doi.org/10.3389/fnut.2022.897028
Stránská, J., Šebela, M., Tarkowski, P., Řehulka, P., Chmelík, J., Popa, I. and Peč, P. 2007. Inhibition of plant amine oxidases by a novel series of diamine derivatives. Biochimie, 89(1), 135–144.
https://doi.org/10.1016/j.biochi.2006.08.001
Thévenot, D. R., Toth, K., Durst, R. A. and Wilson, G. S. 2001. Electrochemical biosensors: recommended definitions and classification. Biosens. Bioelectron., 16(1–2), 121–131.
https://doi.org/10.1016/S0956-5663(01)00115-4
Vinci, G. and Antonelli, M. L. 2002. Biogenic amines: quality index of freshness in red and white meat. Food Control, 13(8), 519–524.
https://doi.org/10.1016/S0956-7135(02)00031-2
Wimmerová, M. and Macholán, L. 1999. Sensitive amperometric biosensor for the determination of biogenic and synthetic amines using pea seedlings amine oxidase: a novel approach for enzyme immobilisation. Biosens. Bioelectron., 14(8–9), 695–702.
https://doi.org/10.1016/S0956-5663(99)00048-2
Wójcik, W., Łukasiewicz, M. and Puppel, K. 2021. Biogenic amines: formation, action and toxicity – a review. J. Sci. Food Agric., 101(7), 2634–2640.
https://doi.org/10.1002/jsfa.10928
Yano, Y., Yokoyama, K., Tamiya, E. and Karube, I. 1996. Direct evaluation of meat spoilage and the progress of aging using biosensors. Anal. Chim. Acta, 320(2–3), 269–276.
https://doi.org/10.1016/0003-2670(95)00543-9
Yoon, H., Park, J. H., Choi, A., Hwang, H.-J. and Mah, J.-H. 2015. Validation of an HPLC analytical method for determination of biogenic amines in agricultural products and monitoring of biogenic amines in Korean fermented agricultural products. Toxicol. Res., 31(3), 299–305.
https://doi.org/10.5487/TR.2015.31.3.299
