Inhibition of N-(carboxymethyl)lysine and N-(carboxyethyl)lysine formation in air-fried beef tenderloins marinated with concentrated cranberry juice

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<p>Food Bioscience 60 (2024) 104336</p><p>Available online 13 May 2024</p><p>2212-4292/© 2024 Elsevier Ltd. All rights are reserved, including those for text and data mining, AI training, and similar technologies.</p><p>Inhibition of Nε-(carboxymethyl)lysine and Nε-(carboxyethyl)lysine</p><p>formation in air-fried beef tenderloins marinated with concentrated</p><p>cranberry juice</p><p>Serap Kılıç Altun a, Mehmet Emin Aydemir a,*, Kasım Takım b, Mustafa Abdullah Yilmaz c,</p><p>Hamza Yalçin d</p><p>a Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Harran University, Şanlıurfa, Turkey</p><p>b Department of Basic Sciences, Faculty of Veterinary, Harran University, Şanlıurfa, Turkey</p><p>c Department of Analytical Chemistry, Faculty of Pharmacy, Dicle University, Diyarbakır, Turkey</p><p>d Department of Biostatistics, Faculty of Agriculture, Harran University, Şanlıurfa, Turkey</p><p>A R T I C L E I N F O</p><p>Keywords:</p><p>Airfryer</p><p>Beef</p><p>Cranberry juice</p><p>Marination</p><p>Nε-(carboxymethyl)lysine</p><p>Nε-(carboxyethyl)lysine</p><p>A B S T R A C T</p><p>The aim of this study was to investigate the effect of marinating beef tenderloin with concentrated cranberry</p><p>juice on the formation of Nε-(carboxymethyl)lysine (CML) and Nε-(carboxyethyl)lysine (CEL). In order to ach-</p><p>ieve this, the concentrated cranberry juice was prepared from cranberry fruit and characterised. Subsequently,</p><p>beef tenderloins were marinated at two different concentrations (25% and 50%) and three different marination</p><p>times (2, 6 and 24 h), after which they were cooked in an airfryer at 200 ◦C for 12 min. Following the cooking</p><p>process, CML, CEL, thiobarbituric acid reactive substances (TBARS) and colour were analysed. It was found that</p><p>concentrated cranberry juice has high phytochemical and bioactivity properties. Cranberry juice was found to be</p><p>high in total phenolic compounds (TPC), total flavonoid compounds (TFC), antioxidant activity and rich in</p><p>bioactive compounds. It was found that cranberry juice significantly altered the colour properties (L*, a*, and b*)</p><p>of raw beef tenderloin samples (p 0.05). 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Marinating</p><p>beef with cranberry juice concentrate may have potentially beneficial</p><p>effects on advanced glycation end products (AGEs) such as Nε-(car-</p><p>boxymethyl)lysine (CML) and Nε-(carboxyethyl)lysine (CEL). Scientific</p><p>research into how CML and CEL levels are affected in beef marinated in</p><p>cranberry juice concentrate can provide valuable information about the</p><p>interaction between the unique compounds in cranberries and the</p><p>complex chemistry that occurs during the cooking process. This study</p><p>aims to determine how CML and CEL levels are affected in red meat</p><p>marinated with cranberry juice concentrate, thus providing valuable</p><p>information about the interaction between the bioactive compounds in</p><p>cranberry juice concentrate and the complex chemistry that occurs</p><p>during the airfry cooking process.</p><p>2. Materials and methods</p><p>2.1. Material, extraction procedures and characterization processes</p><p>2.1.1. Chemical and reagents</p><p>For the preparation of cranberry juice: analytical grade methanol,</p><p>distilled water, extraction solvent (methanol:water, 1:10 v/v) and</p><p>Whatman No. 1 filter paper.</p><p>For the characterization of concentrated cranberry juice: analytical</p><p>grade methanol, ABTS (2,2′-azino-bis (3-ethylbenzothiazoline-6-sul-</p><p>phonic acid) diammonium salt), DPPH (2,2-diphenyl-1-picrylhydrazyl),</p><p>standard phenolic compounds for identification.</p><p>For marinating and cooking of beef tenderloin samples: distilled</p><p>water, sterile containers, baking paper.</p><p>For laboratory analysis of beef tenderloin samples: digital pH meter</p><p>(EDT. GP 353, UK), ELISA kits for Nε-(carboxymethyl)lysine (CML), Nε-</p><p>(carboxyethyl)lysine (CEL) analysis, thiobarbituric acid reactive sub-</p><p>stances (TBARS) ELISA kit (Oxford Biomedical Research, USA) and CS-</p><p>10◦ 8 mm portable digital colorimeter (Tuodapu, Inc., China).</p><p>2.1.2. Collection and preparation of concentrated cranberry juice</p><p>Cranberry (Cornus mas L.) fruit samples were harvested from mid-</p><p>August to the end of September in 2023. All cranberry fruits were</p><p>sampled at the empirically determined stage of full ripeness from the</p><p>same growing region. Samples were collected from an orchard in the</p><p>Uzundere district of Erzurum province, Turkey (40◦32′11″N</p><p>41◦32′54″E). In this way, the same cultivation technique, climate and</p><p>soil conditions (alluvial) were assumed, so that any variations in the</p><p>results due to these factors were ignored in the interpretation. On the</p><p>other hand, as these fruit trees have been subject to organic production</p><p>for many years, no fertilisers or pesticides have been used. Samples were</p><p>processed immediately after harvest. The fresh cranberries were care-</p><p>fully selected, cleaned and then blended for 10 min in a standard</p><p>household blender to make juice. The finished product was blanched for</p><p>5 min at a constant temperature of 90 ◦C. After extracting the remaining</p><p>juice by cloth filtration, it was pasteurised at 80 ◦C for 5 min. The</p><p>cranberry juice was concentrated under vacuum at 50 ◦C in a Heidolph-</p><p>Rotary TLR 10 rotary evaporator (Germany) until it reached 55◦Brix, as</p><p>measured using a refractometer. The concentrated cranberry juice was</p><p>then stored in a sterilised glass bottle of 1-L capacity at a temperature of</p><p>4 ◦C. It was subsequently utilised for the marination of meat (Özen et al.,</p><p>2020).</p><p>2.1.3. Characterization of concentrated cranberry juice</p><p>The concentrated cranberry juice was extracted using two separate</p><p>extraction techniques (methanol and water), each carried out in three</p><p>independent repetitions. The concentrated cranberry juice was extrac-</p><p>ted using methanol and water according to the method of Takım & Işık</p><p>(2020) A falcon tube was filled with 2 mL of concentrated cranberry</p><p>juice, 20 mL of solvent (1:10), and homogenised. It was combined for 24</p><p>h at 25 ◦C and 300 rpm in a double boiler. Whatman No. 1 filter paper</p><p>was used to filter the extracts. Next, the solvents were removed using a</p><p>Heidolph-Rotary TLR 1000 rotary evaporator. The amounts of dry</p><p>extract were calculated. Three independent replicates of the analyses</p><p>were carried out in order to characterise concentrated cranberry juice.</p><p>Total phenolic compounds, total flavonoid compounds, antioxidant ac-</p><p>tivity (DPPH and ABTS) were determined by modification of the</p><p>methods outlined by (Aydemir, Kılıç Altun, & Takım, 2024) .</p><p>2.1.3.1. Quantitative assessment of concentrated cranberry juice’s bioactive</p><p>phytochemicals. The identification of phytochemicals (especially</p><p>phenolic compounds) in concentrated cranberry juice was carried out</p><p>using the analytical technique developed byYilmaz(2020), where a total</p><p>of 53 different standard phenolic compounds were investigated. Refer-</p><p>ence phytochemical standards (53 phytochemicals) were obtained from</p><p>S.K. Altun et al.</p><p>Food Bioscience 60 (2024) 104336</p><p>3</p><p>Sigma-Aldrich (Steinheim, Germany). 1,5-Dicaffeoylquinic acid and the</p><p>internal standards ferulic acid-D3, rutin-D3, and quercetin-D3 were</p><p>purchased from TRC (Toronto, Canada). In this study 53 phytochemicals</p><p>(quinic acid, fumaric acid, gallic acid, malic acid, epigallocatechin,</p><p>protocatechuic acid, catechin, gentisic acid, chlorogenic acid, proto-</p><p>catechuic aldehyde, tannic acid, epigallocatechin gallate, 4-OH benzoic</p><p>acid, epicatechin, vanillic acid, caffeic acid, syringic acid, vanillin,</p><p>syringic aldehyde, daidzin, epicatechin gallate, piceid, ferulic acid,</p><p>p-coumaric acid, sinapic acid, coumarin, salicylic acid, cynaroside,</p><p>miquelianin, rutin, isoquercitrin, hesperidin, o-coumaric acid, genistin,</p><p>rosmarinic acid, ellagic acid, cosmosiin, quercitrin, astragalin, nicoti-</p><p>florin, fisetin, cynarine, daidzein, quercetin, naringenin, luteolin, hes-</p><p>peretin, genistein, apigenin, kaempferol, amentoflavone, chrysin, and</p><p>acacetin) were analysed by LC-MS/MS employing a dual MS instrument</p><p>in conjunction with a Shimadzu HPLC Nexera model. The apparatus</p><p>used for liquid chromatography included a vp column furnace, LC-30 CE</p><p>dual pump, KTO-10AS SIL-30 AC autosampler, and DGU-20A3R deaer-</p><p>ator. A C18 reverse-phase analytical column (Inertsil ODS-4, 150 mm ×</p><p>4.6 mm, 3 μm) was employed for the chromatographic separation.</p><p>Mobile phases of A (water, 5 mM ammonium formate, and 0.1% formic</p><p>acid) and B (methanol, 5 mM ammonium formate, and 0.1% formic</p><p>acid) were used to prepare the elution gradient while the column tem-</p><p>perature was kept constant at 40 ◦C. The injection volume was set at 4 μL</p><p>and the solvent flow rate was fixed at 0.5 mL/min. A Shimadzu model</p><p>LC-MS 8040 mass spectrometer with an ESI source capable of operating</p><p>in triple and quadrupole, negative and positive ionisation modes was</p><p>used to determine the phytochemical composition of the sample.</p><p>LC-MS/MS data acquisition was performed using Lab Solutions software</p><p>(Shimadzu, Kyoto, Japan) to complete the calculations. Multiple Reac-</p><p>tion Monitoring (MRM) mode was used to perform the analysis. Each</p><p>compound was analysed three times. The first analysis was performed</p><p>for quantitative results, while the second and third studies were per-</p><p>formed for confirmation. A DL temperature of 250 ◦C, an interface</p><p>temperature of 350 ◦C, a heat sink temperature of 400 ◦C, a dryer gas</p><p>flow of 15 l/min and a nebuliser gas flow of 3 l/min were the ideal values</p><p>for the mass spectrometer. The formula used to calculate the results after</p><p>integrating the standard deviation data into the LC-MS/MS analysis was</p><p>standard deviation (±) = analyte value result * U value/100. The ana-</p><p>lyte quantity ± uncertainty was reported</p><p>as the quantitative results of</p><p>the LC-MS/MS analyses. The amount of each analyte was multiplied by</p><p>the corresponding U value of the analyte to determine the uncertainty</p><p>values. The analyte uncertainty (U) values presented in Table 2 were</p><p>obtained from the analytical technique validation research of the</p><p>LC-MS/MS method developed by Yılmaz et al. (2020), that was used.</p><p>Table 1</p><p>DPPH and ABTS activity values of concentrated cranberry juice (Mean ± Stan-</p><p>dard Error).</p><p>Concentration amounts</p><p>Extract 1 mg/ml 500 μg/ml 250 μg/</p><p>ml</p><p>ABTS (μg trolox equivalent/g</p><p>dry concentrated</p><p>cranberry juice)</p><p>Methanol 313.83 ±</p><p>13.72</p><p>109.66 ±</p><p>11.70</p><p>76.39 ±</p><p>8.60a</p><p>Water 307.45 ±</p><p>13.60</p><p>98.26 ±</p><p>9.82</p><p>52.69 ±</p><p>6.77b</p><p>DPPH (μg trolox equivalent/</p><p>g dry concentrated</p><p>cranberry juice)</p><p>Methanol 274.31 ±</p><p>12.78</p><p>244.36 ±</p><p>13.60a</p><p>125.03 ±</p><p>5.20a</p><p>Water 285.07 ±</p><p>12.58</p><p>82.45 ±</p><p>8.60b</p><p>46.41 ±</p><p>2.20b</p><p>DPPH: 1,1-Diphenyl-2-picrylhydrazil, ABTS: 2,2-Azino-bis (3-ethylbenzo-thia-</p><p>zoline-6-sulfonic acid, a-b*: Values with different superscripts in the same col-</p><p>umn are statistically different (p</p><p>of TBARS, the method of</p><p>Aydemir et al. (2024a) was modified and applied. The TBARS amounts</p><p>in the samples were estimated using mg MDA/kg.</p><p>2.3.4. Evaluation of Nε–(carboxymethyl) lysine (CML) and Nε-</p><p>(carboxyethyl) lysine (CEL) in beef tenderloin samples</p><p>The OxiSelectTM Nε-(carboxymethyl) lysine (CML) and OxiSelectTM</p><p>Nε-(carboxyethyl) lysine (CEL) Competitive ELISA Kit were employed</p><p>for the analysis of CML and CEL in meat samples (Aydemir et al., 2024a).</p><p>Calculations were performed by generating graphs using the data from</p><p>the control wells, and the output was expressed in μg/g (Aydemir et al.,</p><p>2024a).</p><p>2.4. Statistical analysis</p><p>The characterization analyses for concentrated cranberry juice were</p><p>performed in three separate and independent replicates, while the as-</p><p>sessments for beef tenderloin samples were performed in two separate</p><p>and independent replicates. The fruit juice characterization data set is</p><p>presented as mean ± standard error and includes measurements of meat</p><p>sample composition, pH, colour, TBARS, CEL and CML analyses as well</p><p>as total phenolic content (TPC), total flavonoid content (TFC), ABTS and</p><p>DPPH assays and bioactive phytochemicals. Statistical analyses were</p><p>performed using the general linear model (GLM) with the specified</p><p>equation. The fixed factors in this GLM procedure were the marination</p><p>times (2, 6 and 24 h) and the concentrated cranberry juice concentra-</p><p>tions (25% and 50%), while replicates were treated as random effects.</p><p>Tukey’s test was used for multiple comparisons (p</p><p>to other interaction effects (p</p><p>MDA levels and enhance the activity of antioxidant</p><p>enzymes in rat synaptosomes. This is of significant importance in the</p><p>protection against oxidative stress caused by free radicals. In the case of</p><p>25% concentration, it was observed that the CML value in marinated</p><p>beef tenderloin samples decreased with increasing duration, and the</p><p>average value of the 25%*24h interaction effect was the lowest. Simi-</p><p>larly, when the marinade concentration was increased to 50%, it was</p><p>found that the CML value in beef tenderloin samples decreased with</p><p>increasing duration, and the average value of the 50%*24-h interaction</p><p>effect was the lowest. It is believed that this is due to more bioactive</p><p>compounds being released into the meat as marination time and con-</p><p>centration increase. Indeed, Karatepe et al. (2023) reported that the</p><p>highest marinade absorption was observed in samples marinated for 24</p><p>h. As marinade absorption increases, more bioactive compounds enter</p><p>the beef tenderloin samples, resulting in a more pronounced pH decrease</p><p>(Fig. 2) and significant inhibition of oxidation (Fig. 2). Accelerated in-</p><p>hibition of CML formation will occur due to the pH decrease and a sig-</p><p>nificant decrease will be observed. The critical effect on the rate of the</p><p>Maillard reaction is already known (Vlassara & Uribarri, 2004). Due to</p><p>the significant inhibition of oxidation, there will be less CML formation.</p><p>In addition, Fig. 3 shows a strong positive correlation between TBARS</p><p>and CML. Consistent with our findings, a positive relationship between</p><p>CML and oxidation is reported (Aydemir, Kılıç Altun, & Takım, 2024).</p><p>The effect of the interaction on the dependent variable CEL was not</p><p>significant (p ≥ 0.05) (Table 3). In addition, the level of CEL in the beef</p><p>tenderloin samples was higher than the level of CML. While concen-</p><p>trated cranberry juice significantly inhibited CML formation in mari-</p><p>nated beef tenderloin samples, it did not affect CEL formation. This may</p><p>be explained by the fact that methylglyoxal (MGO) (a precursor of CEL)</p><p>is formed at higher levels than glyoxal (GO) (a precursor of CML), and</p><p>the bioactive compounds present in concentrated cranberry juice do not</p><p>bind to the GO formed at high levels, resulting in MGO. Indeed, Liu et al.</p><p>(2017) reported that the MGO content in the lysine-glucose system was</p><p>Fig. 3. Graphical representation of the correlation heatmap and biplot PCA analysis including 25% and 50% for all variables. *: p 0.05), they were significant for the a* and b* values (p 0.05), they</p><p>were significant for the a* and b* values (p</p><p>decreases could be attributed to the reduction in water content,</p><p>increased protein denaturation and the formation of brown pigments</p><p>(metmyoglobin) during the cooking process (Del Pulgar, Gázquez, &</p><p>Ruiz-Carrascal, 2012).</p><p>Although concentrated cranberry juice exhibits a bright red hue on</p><p>its own, the darker (purplish-red) colour observed in meats, particularly</p><p>when marinated, is likely due to the partial colour change of anthocy-</p><p>anin ions from red to blue. This is supported by the pH alteration upon</p><p>marination, as reported by von Elbe and Schwartz (1981). The sub-</p><p>stantial alteration in the colour parameters of meat samples marinated</p><p>with concentrated cranberry juice, resulting in darker colour tones, can</p><p>be attributed to the masking of the brightness and intensity of newly</p><p>formed meat colour pigments. (Lau et al., 2021).</p><p>3.8. Statistical evaluation of the data</p><p>3.8.1. The results of the experiment in conjunction with the principal</p><p>component analyses of the data</p><p>The correlation graph (correlogram) illustrating the interrelation-</p><p>ship between TBARS and CML is presented in Fig. 3. A highly significant</p><p>positive correlation (R = 0.854, p</p><p>have revealed that concentrated cranberry</p><p>juice contains high levels of total phenolic content, total flavonoid</p><p>content, and antioxidant properties, indicating the presence of various</p><p>bioactive compounds. It has been demonstrated that the bioactive</p><p>components present in concentrated cranberry juice exert a significant</p><p>inhibitory effect on the formation of Nε-(carboxymethyl)lysine (CML) in</p><p>beef tenderloin samples. As the concentration and duration of the</p><p>marinade increase, a significant decrease in CML levels is observed.</p><p>Furthermore, it has been demonstrated that the formation of Nε-(car-</p><p>boxyethyl)lysine (CEL) is not inhibited, but rather, its stability is</p><p>ensured.</p><p>The marination of meat with concentrated cranberry juice has</p><p>resulted in a reduction in the formation of CML to low levels, with in-</p><p>hibition observed at 1.2 μg/g, representing a reduction of up to 12.39</p><p>μg/g. Moreover, the marination process has not resulted in significant</p><p>alterations to the colour values of the meat, but has significantly reduced</p><p>the TBARS value due to its high free radical scavenging capacity. A</p><p>positive correlation was observed between CML levels and thio-</p><p>barbituric acid reactive substances (TBARS), indicating that oxidation</p><p>processes contribute to CML formation. Furthermore, a positive corre-</p><p>lation was observed between CML levels and pH values, indicating that</p><p>CML formation is slowed down at low pH values.</p><p>In conclusion, the results of this study demonstrate that marinating</p><p>meat with concentrated cranberry juice significantly inhibits the for-</p><p>mation of CML and stabilises the formation of CEL. The results indicate</p><p>that marinating the meat with a cranberry vinegar-based marinade (at a</p><p>Fig. 6. Hierarchical clustering analysis with a heatmap presentation for the</p><p>numerical data obtained from the tenderloin experiment. C (L*, a*, and b*):</p><p>Color values of cooked groups, R (L*, a*, and b*): Color values of raw groups,</p><p>CML: Nε-(carboxymethyl) lysine, CEL: Nε-(carboxyethyl) lysine, TBARS: Thio-</p><p>barbituric acid reactive substances, h: Hour. (For interpretation of the refer-</p><p>ences to colour in this figure legend, the reader is referred to the Web version of</p><p>this article.)</p><p>S.K. Altun et al.</p><p>Food Bioscience 60 (2024) 104336</p><p>11</p><p>concentration of 50% for 24 h) is an effective strategy to prevent the</p><p>formation of advanced glycation end products (AGEs) in the meat. It is</p><p>recommended that further research be conducted in order to optimise</p><p>the marination process and elucidate the underlying mechanisms</p><p>responsible for the observed inhibition of CML formation. Furthermore,</p><p>the potential synergistic effects of cranberry juice with other natural</p><p>antioxidants or food additives could enhance the efficacy of AGE inhi-</p><p>bition and expand the application of this approach to a wider range of</p><p>meat and meat products. Overall, the findings presented here under-</p><p>score the importance of harnessing the bioactive properties of natural</p><p>ingredients, such as concentrated cranberry juice, in food processing to</p><p>promote health and well-being. By integrating these insights into meat</p><p>processing practices, we can make significant progress towards the</p><p>development of safer and healthier food options for consumers</p><p>worldwide.</p><p>CRediT authorship contribution statement</p><p>Serap Kılıç Altun: Writing – review & editing, Writing – original</p><p>draft, Validation, Methodology, Investigation, Formal analysis, Data</p><p>curation, Conceptualization. Mehmet Emin Aydemir: Writing – review</p><p>& editing, Writing – original draft, Methodology, Investigation, Formal</p><p>analysis, Data curation, Conceptualization. Kasım Takım: Writing –</p><p>review & editing, Methodology, Formal analysis. Mustafa Abdullah</p><p>Yilmaz: Writing – review & editing, Methodology, Formal analysis.</p><p>Hamza Yalçın: Writing – review & editing, Methodology, Formal</p><p>analysis.</p><p>Declaration of competing interest</p><p>The authors declare that they have no known competing financial</p><p>interests or personal relationships that could have appeared to influence</p><p>Fig. 7. Slope charts representation of the relationships between the variables at 25% and 50% separately. C (L*, a*, and b*): Color values of cooked groups, R (L*,</p><p>a*, and b*): Color values of raw groups, CML: Nε-(carboxymethyl) lysine, CEL: Nε-(carboxyethyl) lysine. TBARS: Thiobarbituric acid reactive substances, h: Hour.</p><p>(For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)</p><p>Fig. 8. Chord diagram representation of the relationships between the variables at 25% and 50% separately. C (L*, a*, and b*): Color values of cooked groups, R</p><p>(L*, a*, and b*): Color values of raw groups, CML: Nε-(carboxymethyl) lysine, CEL: Nε-(carboxyethyl) lysine, TBARS: Thiobarbituric acid reactive substance. (For</p><p>interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)</p><p>S.K. Altun et al.</p><p>Food Bioscience 60 (2024) 104336</p><p>12</p><p>the work reported in this paper The author is an Editorial Board</p><p>Member/Editor-in-Chief/Associate Editor/Guest Editor for [Journal</p><p>name] and was not involved in the editorial review or the decision to</p><p>publish this article.</p><p>Data availability</p><p>Data will be made available on request.</p><p>Appendix A. Supplementary data</p><p>Supplementary data to this article can be found online at https://doi.</p><p>org/10.1016/j.fbio.2024.104336.</p><p>References</p><p>Abdi, F., Tabibiazar, M., Taghvimi, A., & Ghorbani, M. (2021). Effect of tannic and gallic</p><p>acid on glycation of egg white protein and formation N-(Carboxyl methyl) lysine.</p><p>Food Bioscience, 43, Article 101245. https://doi.org/10.1016/j.fbio.2021.101245</p><p>Abeywickrama, G., Debnath, S. C., Ambigaipalan, P., & Shahidi, F. (2016). 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