Abstract
The microbiological contamination of food causes concern for public health due to the pathogenic action of microorganisms and the increasing of antimicrobial resistance observed in bacterial strains. This work considers the use of fluorescence spectroscopy to study the effects of the presence of microorganisms in the chicken’s meat and therefore, how the detection of this presence can help on food safety. The fluorescence of organic boneless and skinless chicken breast pieces contaminated with variable concentrations of E. coli cells inoculated in meat (104, 105, 106, and 107 cells/mL) was measured with excitations at 340 and 410 nm. Raman spectra were obtained to investigate into conformational changes in the collagen structures, from samples kept for 48 h at 25 °C (non-contaminated and contaminated with E. coli, 105 and 107 cells/mL). Protoporphyrin IX fluorescence lifetime was measured in the function of an increased number of E. coli cells. The obtained results of E. coli were compared to the ones of Salmonella and Campylobacter contaminations (106 cells/mL). Some uncommon aspects were found in the spectra of the contaminated meat: enlargement of the collagen band at 400 nm; increase in free reduced nicotinamide adenine dinucleotide fluorescence intensity around 505 nm; and decrease of flavin emission band. A shortening in the porphyrin emission lifetime (from ~ 10 ns for uncontaminated meat to ~ 5 ns) was observed, showing a quenching process for the meat contaminated with E. coli. The presence of coproporphyrin emission band was observed in the samples contaminated with Salmonella. The singularities observed in PpIX fluorescence spectroscopy for E. coli and Salmonella can be used to obtain a quick detection method of pathogenic bacteria.
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References
Adamsen CE, Moller JKS, Laursen K, Olsen K, Skibsted LH (2006) Zn-porphyrin formation in cured meat products: effect of added salt and nitrite. Meat Sci 72(4):672–679. https://doi.org/10.1016/j.meatsci.2005.09.017
Afonso SG, de Salamanca RE, Batlle AMD (1999) The photodynamic and non-photodynamic actions of porphyrins. BJMBR 32(3):255–266
Allos BM, Blaser MJ (1995) Campylobacter jejuni and the expanding spectrum of related infections. Clin Infect Dis 20(5):1092–1099. https://doi.org/10.1093/clinids/20.5.1092
Argyri AA, Jarvis RM, Wedge D, Xu Y, Panagou EZ, Goodacre R, Nychas G-JE (2013) A comparison of Raman and FT-IR spectroscopy for the prediction of meat spoilage. Food Control 29(2):461–470. https://doi.org/10.1016/j.foodcont.2012.05.040
Belluco S, Barco L, Roccato A, Ricci A (2016) Escherichia coli and Enterobacteriaceae counts on poultry carcasses along the slaughterline: a systematic review and meta-analysis. Food Control 60:269–280. https://doi.org/10.1016/j.foodcont.2015.07.033
Breuch R, Klein D, Siefke E, Hebel M, Herbert U, Wickleder C, Kaul P (2020) Differentiation of meat-related microorganisms using paper-based surface-enhanced Raman spectroscopy combined with multivariate statistical analysis. Talanta 219:121315. https://doi.org/10.1016/j.talanta.2020.121315
Cherng SH, Xia QS, Blankenship LR, Freeman JP, Wamer WG, Howard PC, Fu PP (2005) Photodecomposition of retinyl palmitate in ethanol by UVA light-formation of photodecomposition products, reactive oxygen species, and lipid peroxides. Chem Res Toxicol 18(2):129–138. https://doi.org/10.1021/tx049807l
Courrol LC, Samad RE (2018) Determination of chicken meat contamination by porphyrin fluorescence. J Lumin 199:67–70. https://doi.org/10.1016/j.jlumin.2018.03.006
Courrol, LC, Vallim MA (2019) 2019 SBFOTON International Optics and Photonics Conference (SBFOTON IOPC), Fluorescence profile of chicken meat contaminated with E. coli Proceedings Paper ConferênciaConferência: SBFoton International Optics and Photonics Conference (SBFoton IOPC)
Cuong NV, Padungtod P, Thwaites G, Carrique-Mas JJ (2018) Antimicrobial usage in animal production: a review of the literature with a focus on low- and middle-income countries. Antibiotics (Basel) 7(3). https://doi.org/10.3390/antibiotics7030075
De Gelder J, De Gussem K, Vandenabeele P, Moens L (2007) Reference database of Raman spectra of biological molecules. J Raman Spectrosc 38(9):1133–1147. https://doi.org/10.1002/jrs.1734
De Maere H, Fraeye I, De Mey E, Dewulf L, Michiels C, Paelinck H, Chollet S (2016) Formation of naturally occurring pigments during the production of nitrite-free dry fermented sausages. Meat Sci 114:1–7. https://doi.org/10.1016/j.meatsci.2015.11.024
Deng L, Li Y, Yan XP, Xiao J, Ma C, Zheng J et al (2015) Ultrasensitive and highly selective detection of bioaccumulation of methyl-mercury in fish samples via Ag-0/Hg-0 amalgamation. Anal Chem 87(4):2452–2458. https://doi.org/10.1021/ac504538v
Dhanasekar NN, Rahul GR, Narayanan KB, Raman G, Sakthivel N (2015) Green chemistry approach for the synthesis of gold nanoparticles using the fungus Alternaria sp. J Microbiol Biotechnol 25(7):1129–1135. https://doi.org/10.4014/jmb.1410.10036
Dufour E (2011) Recent advances in the analysis of dairy product quality using methods based on the interactions of light with matter. Int J Dairy Technol 64(2):153–165. https://doi.org/10.1111/j.1471-0307.2010.00665.x
Durek J, Frohling A, Bolling J, Thomasius R, Durek P, Schluter OK (2016) Non-destructive mobile monitoring of microbial contaminations on meat surfaces using porphyrin fluorescence intensities. Meat Sci 115:1–8. https://doi.org/10.1016/j.meatsci.2015.12.022
Evans EW, Dodson CA, Maeda K, Biskup T, Wedge CJ, Timmel CR (2013) Magnetic field effects in flavoproteins and related systems. Interface Focus 3(5):20130037. https://doi.org/10.1098/rsfs.2013.0037
Galban J, Sanz-Vicente I, Navarro J, de Marcos S (2016) The intrinsic fluorescence of FAD and its application in analytical chemistry: a review. Methods Appl Fluoresc 4(4). https://doi.org/10.1088/2050-6120/4/4/042005
Gasior-Glogowska M, Komorowska M, Hanuza J, Ptak M, Kobielarz M (2010) Structural alteration of collagen fibres-spectroscopic and mechanical studies. Acta Bioeng Biomech 12(4):55–62
Gogoi SK, Gopinath P, Paul A, Ramesh A, Ghosh SS, Chattopadhyay A (2006) Green fluorescent protein-expressing Escherichia coli as a model system for investigating the antimicrobial activities of silver nanoparticles. Langmuir 22(22):9322–9328. https://doi.org/10.1021/la060661v
Gross M (2013) Antibiotics in crisis. Curr Biol 23(24):R1063–R1065. https://doi.org/10.1016/j.cub.2013.11.057
Hille R, Miller S, Palfey B (2013) Handbook of flavoproteins, 2 Complex flavoproteins, dehydrogenases and physical methods. De Gruyter, Boston, Berlin
Ishikawa H, Kawabuchi T, Kawakami Y, Sato M, Numata M, Matsumoto K (2007) Formation of zinc protoporphyrin IX and protoporphyrin IX from oxymyoglobin in porcine heart mitochondria. Food Sci Technol Res 13(1):85–88. https://doi.org/10.3136/fstr.13.85
Jaafreh S, Breuch R, Gunther K, Kreyenschmidt J, Kaul P (2018) Rapid poultry spoilage evaluation using portable fiber-optic Raman spectrometer. Food Anal Methods 11(8):2320–2328. https://doi.org/10.1007/s12161-018-1223-0
Kao Y-T, Saxena C, He T-F, Guo L, Wang L, Sancar A, Zhong D (2008) Ultrafast dynamics of flavins in five redox states. J Am Chem Soc 130(39):13132–13139. https://doi.org/10.1021/ja8045469
Kiermeier A, Jenson I, Sumner J (2015) Risk assessment of Escherichia coli O157 illness from consumption of hamburgers in the United States made from Australian manufacturing beef. Risk Anal 35(1):77–89. https://doi.org/10.1111/risa.12248
Kim J, Gherasim C, Banerjee R (2008) Decyanation of vitamin B-12 by a trafficking chaperone. Proc Natl Acad Sci U S A 105(38):14551–14554. https://doi.org/10.1073/pnas.0805989105
Kochevar IE (1987) Mechanisms of drug photosensitization. Photochem Photobiol 45(6):891–895. https://doi.org/10.1111/j.1751-1097.1987.tb07899.x
Leblanc L, Dufour E (2002) Monitoring the identity of bacteria using their intrinsic fluorescence. FEMS Microbiol Lett 211(2):147–153. https://doi.org/10.1111/j.1574-6968.2002.tb11217.x
Martinez MG, Bullock AJ, MacNeil S, Rehman IU (2019) Characterisation of structural changes in collagen with Raman spectroscopy. Appl Spectrosc Rev 54(6):509–542. https://doi.org/10.1080/05704928.2018.1506799
Morgan WT, Smith A, Koskelo P (1980) The interaction of human serum albumin and hemopexin with porphyrins. Biochim Biophys Acta 624(1):271–285. https://doi.org/10.1016/0005-2795(80)90246-9
Movasaghi Z, Rehman S, Rehman IU (2007) Raman spectroscopy of biological tissues. Appl Spectrosc Rev 42(5):493–541. https://doi.org/10.1080/05704920701551530
Narayanan M, Singh VR, Kodali G, Moravcevic K, Stanley RJ (2017) An ethenoadenine FAD analog accelerates UV dimer repair by DNA photolyase. Photochem Photobiol 93(1):343–354. https://doi.org/10.1111/php.12684
Natarajan P, Raja C (2001) Novel features of the interpolymer self-organisation behaviour investigated using covalently linked protoporphyrin IX as fluorescent probe in the macromolecules. Eur Polym J 37(11):2207–2211. https://doi.org/10.1016/S0014-3057(01)00127-6
Nguyen TT, Gobinet C, Feru J, Brassart-Pasco S, Manfait M, Piot O (2012) Characterization of type I and IV collagens by Raman microspectroscopy: identification of spectral markers of the dermo-epidermal junction. SPECTROSC-INT J 27(5–6):421–427. https://doi.org/10.1155/2012/686183
Papuc C, Goran GV, Predescu CN, Nicorescu V (2017) Mechanisms of oxidative processes in meat and toxicity induced by postprandial degradation products: a review. Compr Rev Food Sci Food Saf 16(1):96–123. https://doi.org/10.1111/1541-4337.12241
Polmickaite-Smirnova E, Bagdonas S, Anusevicius Z (2019) Sensitization of Salmonella enterica with 5-aminolevulinic acid-induced endogenous porphyrins: a spectroscopic study. Photochem Photobiol Sci 18(11):2730–2739. https://doi.org/10.1039/c9pp00200f
Pu Y, Wang WB, Alfano RR (2013) Optical detection of meat spoilage using fluorescence spectroscopy with selective excitation wavelength. Appl Spectrosc 67(2):210–213. https://doi.org/10.1366/12-06653
Pu Y, Wang WB, Alfano RR (2015) Spoilage of foods monitored by native fluorescence spectroscopy with selective excitation wavelength. Paper presented at the Conference on Optics and Biophotonics in Low-Resource Settings, San Francisco, CA
Rehman AU, Anwer AG, Gosnell ME, Mahbub SB, Liu GZ, Goldys EM (2017) Fluorescence quenching of free and bound NADH in HeLa cells determined by hyperspectral imaging and unmixing of cell autofluorescence. Biomed Opt Express 8(3):1488–1498. https://doi.org/10.1364/boe.8.001488
Ricchelli F, Gobbo S, Moreno G, Salet C, Brancaleon L, Mazzini A (1998) Photophysical properties of porphyrin planar aggregates in liposomes. Eur J Biochem 253(3):760–765. https://doi.org/10.1046/j.1432-1327.1998.2530760.x
Rouger A, Tresse O, Zagorec M (2017) Bacterial contaminants of poultry meat: sources, species, and dynamics. Microorganisms 5(3). https://doi.org/10.3390/microorganisms5030050
Royer CA, Alpert B (1987) Porphyrin dynamics in the heme-pockets of myoglobin and hemoglobin. Chem Phys Lett 134(5):454–460. https://doi.org/10.1016/0009-2614(87)87172-5
Samapundo S, de Baenst I, Aerts M, Cnockaert M, Devlieghere F, Van Damme P (2019) Tracking the sources of psychrotrophic bacteria contaminating chicken cuts during processing. Food Microbiol 81:40–50. https://doi.org/10.1016/j.fm.2018.06.003
Sicchieri LB, Da Silva MN, Samad RE, Courrol LC (2018) Can measurement of the fluorescence lifetime of extracted blood PPIX predict atherosclerosis? J Lumin 195:176–180. https://doi.org/10.1016/j.jlumin.2017.11.014
Sowoidnich K, Kronfeldt H-D (2012) Shifted excitation Raman difference spectroscopy at multiple wavelengths for in-situ meat species differentiation. Appl Phys B Lasers Opt 108(4):975–982. https://doi.org/10.1007/s00340-012-5160-0
Tan C, Guo L, Ai Y, Li J, Wang L, Sancar A, Luo Y, Zhong D (2014) Direct determination of resonance energy transfer in photolyase: structural alignment for the functional state. J Phys Chem A 118(45):10522–10530. https://doi.org/10.1021/jp504349b
Turlin E, Heuck G, Brandeo MIS, Szili N, Mellin JR, Lange N, Wandersman C (2014) Protoporphyrin (PPIX) efflux by the MacAB-TolC pump in Escherichia coli. Microbiologyopen 3(6):849–859. https://doi.org/10.1002/mbo3.203
Varnado CL, Goodwin DC (2004) System for the expression of recombinant hemoproteins in Escherichia coli. Protein Expr Purif 35(1):76–83. https://doi.org/10.1016/j.pep.2003.12.001
Wakamatsu J-i, Okui J, Hayashi N, Nishimura T, Hattori A (2007) Zn protoporphyrin IX is formed not from heme but from protoporphyrin IX. Meat Sci 77(4):580–586. https://doi.org/10.1016/j.meatsci.2007.05.008
Wakamatsu J-i, Odagiri H, Nishimura T, Hattori A (2009) Quantitative determination of Zn protoporphyrin IX, heme and protoporphyrin IX in Parma ham by HPLC. Meat Sci 82(1):139–142. https://doi.org/10.1016/j.meatsci.2008.12.011
Wakamatsu J-i, Hayashi N, Nishimura T, Hattori A (2010) Nitric oxide inhibits the formation of zinc protoporphyrin IX and protoporphyrin IX. Meat Sci 84(1):125–128. https://doi.org/10.1016/j.meatsci.2009.08.036
Wakamatsu J, Akter M, Honma F, Hayakawa T, Kumura H, Nishimura T (2019) Optimal pH of zinc protoporphyrin IX formation in porcine muscles: effects of muscle fiber type and myoglobin content. [Article]. LWT-Food Sci Technol 101:599–606. https://doi.org/10.1016/j.lwt.2018.11.040
Wang HH, Zhang XX, Wang GY, Jia K, Xu XL, Zhou GH (2017) Bacterial community and spoilage profiles shift in response to packaging in yellow-feather broiler, a highly popular meat in Asia. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.02588
Whang K, Peng IC (1988) Electron-paramagnetic resonance studies of the effectiveness of myoglobin and its derivatives as photosensitizers in singlet oxygen generation. J Food Sci 53(6):1863. https://doi.org/10.1111/j.1365-2621.1988.tb07862.x
Wos ML, Pollard PC (2009) Cellular nicotinamide adenine dinucleotide (NADH) as an indicator of bacterial metabolic activity dynamics in activated sludge. Water Sci Technol 60(3):783–791. https://doi.org/10.2166/wst.2009.393
Zettel V, Ahmad MH, Beltramo T, Hermannseder B, Hitzemann A, Nache M, Paquet-Durand O, Schöck T, Hecker F, Hitzmann B (2016a) Supervision of food manufacturing processes using optical process analyzers-an overview. [Review]. Chembioeng Rev 3(5):219–228. https://doi.org/10.1002/cben.201600013
Zettel V, Ahmad MH, Hitzemann A, Nache M, Paquet-Durand O, Schock T et al (2016b) Optical process analyzers in the food industry. Chem Ing Tech 88(6):735–745. https://doi.org/10.1002/cite.201500097
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This work was supported by the São Paulo Research Foundation (grant numbers 2017/23686-6 and 2015/04400-9).
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Courrol, L.C., Vallim, M.A. Spectroscopic Analysis of Chicken Meat Contaminated with E. coli, Salmonella, and Campylobacter. Food Anal. Methods 14, 512–524 (2021). https://doi.org/10.1007/s12161-020-01888-z
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DOI: https://doi.org/10.1007/s12161-020-01888-z