Functional electrospun nanofibers for multimodal sensitive detection of biogenic amines in food via a simple dipstick assay
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Electrospun nanofibers (ENFs) are promising materials for rapid diagnostic tests like lateral flow assays and dipsticks because they offer an immense surface area while excluding minimal volume, a variety of functional surface groups, and can entrap functional additives within their interior. Here, we show that ENFs on sample pads are superior in comparison to standard polymer membranes for the optical detection of biogenic amines (BAs) in food using a dipstick format. Specifically, cellulose acetate (CA) fibers doped with 2 mg/mL of the chromogenic and fluorogenic amine-reactive chameleon dye Py-1 were electrospun into uniform anionic mats. Those extract cationic BAs from real samples and Py-1 transduces BA concentrations into a change of color, reflectance, and fluorescence. Dropping a BA sample onto the nanofiber mat converts the weakly fluorescent pyrylium dye Py-1 into a strongly red emitting pyridinium dye. For the first time, a simple UV lamp excites fluorescence and a digital camera acts as detector. The intensity ratio of the red to the blue channel of the digital image is dependent on the concentration of most relevant BAs indicating food spoilage from 10 to 250 μM. This matches the permitted limits for BAs in foods and no false positive signals arise from secondary and tertiary amines. BA detection in seafood samples was also demonstrated successfully. The nanofiber mat dipsticks were up to sixfold more sensitive than those using a polymer membrane with the same dye embedded. Hence, nanofiber-based tests are not only superior to polymer-based dipstick assays, but will also improve the performance of established tests related to food safety, medical diagnostics, and environmental testing.
KeywordsBiogenic amines Electrospun nanofibers Rapid diagnostic Food analysis Fluorescence Dipstick
NY and AD gratefully acknowledge support by the DFG and the Russian Ministry of Education for project 16.674.2016/DAAD and 16.751.2016/DAAD.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- 1.Erim FB. Recent analytical approaches to the analysis of biogenic amines in food samples. Trends Anal Chem. 2013; https://doi.org/10.1016/j.trac.2013.05.018.
- 2.Kalac P, Gloria MBA. Biogenic amines in cheeses, wines, beers and sauerkraut. In: Dandrifosse G, editor. Biological Aspects of Biogenic Amines, Polyamines and Conjugates. Scarborough: Research Signpost; 2009. pp. 267–310. http://www.ressign.com/UserBookDetail.aspx?bkid=873&catid=208
- 3.Fogel WA, Lewinski A, Jochem J. Histamine in food: is there anything to worry about? Biochem Soc Trans. 2007; https://doi.org/10.1042/BST0350349.
- 4.Özdestan Ö, Üren A. A method for benzoyl chloride derivatization of biogenic amines for high performance liquid chromatography. Talanta. 2009; https://doi.org/10.1016/j.talanta.2009.02.001.
- 5.He L, Xu Z, Hirokawa T, Shena L. Simultaneous determination of aliphatic, aromatic and heterocyclic biogenic amines without derivatization by capillary electrophoresis and application in beer analysis. J Chromatogr A. 2017; https://doi.org/10.1016/j.chroma.2016.12.067.
- 6.Önal AA. Review: current analytical methods for the determination of biogenic amines in foods. Food Chem. 2007; https://doi.org/10.1016/j.foodchem.2006.08.028.
- 7.Marcobal A, Polo MC, Martín-Alvarez PJ, Moreno-Arribas MV. Biogenic amine content of red Spanish wines: comparison of a direct ELISA and an HPLC method for the determination of histamine in wines. Food Res Int. 2005; https://doi.org/10.1016/j.foodres.2004.10.008.
- 8.Luo L, ZL X, Yang JY, Xiao ZL, Li YJ, Beier RC, et al. Synthesis of novel haptens and development of an enzyme-linked immunosorbent assay for quantification of histamine in foods. J Agric Food Chem. 2014; https://doi.org/10.1021/jf504689x.
- 9.Bidmanova S, Steiner MS, Stepan M, Vymazalova K, Michael A, Gruber M, et al. Enzyme-based test strips for visual or photographic detection and quantitation of gaseous sulfur mustard. Anal Chem. 2016; https://doi.org/10.1021/acs.analchem.6b01272.
- 10.Khairy GM, Azab HA, El-Korashy SA, Steiner MS, Duerkop A. Validation of a fluorescence sensor Microtiterplate for biogenic amines in meat and cheese. J Fluoresc. 2016; https://doi.org/10.1007/s10895-016-1885-1.
- 11.Huang X, Li Z, Zou X, Shi J, Mao H, Zhao J, et al. Detection of meat-borne trimethylamine based on nanoporous colorimetric sensor arrays. Food Chem. 2016; https://doi.org/10.1016/j.foodchem.2015.11.041.
- 12.Diaz YJ, Page ZA, Knight AS, Treat NJ, Hemmer JR, Hawker CJ, et al. A versatile and highly selective colorimetric sensor for the detection of amines. Chem Eur J. 2017; https://doi.org/10.1002/chem.201700368.
- 13.Schaude C, Meindl C, Fröhlich E, Attard J, Mohr GJ. Developing a sensor layer for the optical detection of amines during food spoilage. Talanta. 2017; https://doi.org/10.1016/j.talanta.2017.04.029.
- 14.Nedeljko P, Turel M, Lobnik A. Hybrid sol-gel based sensor layers for optical determination of biogenic amines. Sens Actuat B. 2017; https://doi.org/10.1016/j.snb.2017.02.011.
- 15.Sutarlie L, Yang KL. Colorimetric responses of transparent polymers doped with metal phthalocyanine for detecting vaporous amines. Sens Actuat B. 2008; https://doi.org/10.1016/j.snb.2008.07.011.
- 16.Roales J, Pedrosa JM, Guillén MG, Lopes-Costa T, Pinto SMA, Calvete MJF, et al. Optical detection of amine vapors using ZnTriad porphyrin thin films. Sens Actuat B. 2015; https://doi.org/10.1016/j.snb.2014.12.080.
- 17.Wöllner K, Vollprecht M, Leopold N, Kasper M, Busche S, Gauglitz G. Interaction behaviour of a PDMS-calixarene system and polar analytes characterised by microcalorimetry and spectroscopic methods. Anal Bioanal Chem. 2007; https://doi.org/10.1007/s00216-007-1600-9.
- 18.Rawat KA, Bhamore JR, Singhal RK, Kailas SK. Microwave assisted synthesis of tyrosine protected gold nanoparticles for dual (colorimetric and fluorimetric) detection of spermine and spermidine in biological samples. Biosens Bioelectron. 2017; https://doi.org/10.1016/j.bios.2016.07.069.
- 19.Chopra S, Singh A, Venugopalan P, Singh N, Kaur N. Organic nanoparticles for visual detection of Spermidine and Spermine in vapors and aqueous phase. ACS Sustain Chem Eng. 2016; https://doi.org/10.1021/acssuschemeng.6b01295.
- 20.El-Nour KMA, Salam ETA, Soliman HM, Orabi AS. Gold nanoparticles as a direct and rapid sensor for sensitive analytical detection of biogenic amines. Nanoscale Res Lett. 2017; https://doi.org/10.1186/s11671-017-2014-z.
- 21.Steiner MS, Meier RJ, Duerkop A, Wolfbeis OS. Chromogenic sensing of biogenic amines using a chameleon probe and the red–green–blue readout of digital camera images. Anal Chem. 2010; https://doi.org/10.1021/ac102029j.
- 22.Matlock-Colangelo L, Baeumner AJ. Biologically inspired Nanofibers for use in translational bioanalytical systems. Ann Rev Anal Chem. 2014; https://doi.org/10.1146/annurev-anchem-071213-020035.
- 23.Mercante LA, Scagion VP, Migliorini FL, Mattoso LHC, Correa DS. Electrospinning-based (bio)sensors for food and agricultural applications: a review. Trends Anal Chem. 2017; https://doi.org/10.1016/j.trac.2017.04.004.
- 24.Azab HA, El-Korashy SA, Anwar ZM, Khairy GM, Duerkop A. Reactivity of a luminescent “off-on” pyrylium dye towards various classes of amines and its use in a fluorescence sensor microtiter plate for environmental samples. J Photochem Photobiol A. 2012; https://doi.org/10.1016/j.jphotochem.2012.05.029.
- 25.Wetzl BK, Yarmoluk SM, Craig DB, Wolfbeis OS. Chameleon labels for staining and quantifying proteins. Angew Chem Int Ed. 2004; https://doi.org/10.1002/anie.200460508.
- 26.Steiner MS, Meier RJ, Spangler C, Duerkop A, Wolfbeis OS. Determination of biogenic amines by capillary electrophoresis using a chameleon-type of fluorescent stain. Microchim Acta. 2009; https://doi.org/10.1007/s00604-009-0247-y.
- 27.Caro B, Guen-Robin FL, Salmain M, Jaouen G. 4-Benchrotrenyl pyrylium salts as protein organometallic labelling reagents. Tetrahedron. 2000; https://doi.org/10.1016/S0040-4020(99)00947-3.
- 28.AOAC. AOAC Official Methods of Analysis. 16th ed. Washington; AOAC, 1995. Method 35.1.32.Google Scholar
- 29.Stadnik J, Dolatowski ZJ. Biogenic amines in meat and fermented meat products. Acta Sci Pol Technol Aliment. 2010;9:251–63.Google Scholar
- 30.Azab HA, El-Korashy SA, Anwar ZM, Khairy GM, Steiner MS, Duerkop A. High-throughput sensor microtiter plate for determination of biogenic amines in sea food using fluorescence or eye-vision. Analyst. 2011; https://doi.org/10.1039/C1AN15049A.
- 31.Alonso-Lomillo MA, Dominguez-Renedo O, Matos P, Arcos-Martinez MJ. Disposable biosensors for determination of biogenic amines. Anal Chim Acta. 2010; https://doi.org/10.1016/j.aca.2010.03.012.
- 32.Schaude C, Meindl C, Fröhlich E, Attard J, Mohr GJ. Developing a sensor layer for the optical detection of amines during food spoilage. Talanta [Internet]. 2017;170(February):481–7. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0039914017304551 CrossRefGoogle Scholar
- 33.Wang Z, Liu F, Evolution LC. Of biogenic amine concentrations in foods through their induced chemiluminescence inactivation of layered double hydroxide nanosheet colloids. Biosens Bioelectron. 2014; https://doi.org/10.1016/j.bios.2014.04.013.
- 34.Omanovic-Miklicanin E, Valzacchi S. Development of new chemiluminescence biosensors for determination of biogenic amines in meat. Food Chem. 2017; https://doi.org/10.1016/j.foodchem.2017.05.031.
- 35.Tseng S, Li S, Yi S, Sun AY, Gao D, Wan D. Food quality monitor: paper-based plasmonic sensors prepared through reversal nanoimprinting for rapid detection of biogenic amine odorants. ACS Appl Mater Interfaces. 2017; https://doi.org/10.1021/acsami.7b00115.