Effect of Olive Mill Wastewater Phenol Compounds on Reactive

Sep 23, 2014 - Thermal processing and Maillard reaction (MR) affect the nutritional and sensorial qualities of milk. In this paper an olive mill waste...
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Effect of Olive Mill Wastewater Phenol Compounds on Reactive Carbonyl Species and Maillard Reaction End-Products in UltrahighTemperature-Treated Milk Antonio Dario Troise,†,§ Alberto Fiore,§ Antonio Colantuono,§ Smaro Kokkinidou,# Devin G. Peterson,# and Vincenzo Fogliano*,† †

Food Quality and Design Group, Wageningen University and Research Centre, P.O. Box 8129, 6700 EV Wageningen, The Netherlands § Department of Agriculture and Food Science, University of Naples “Federico II”, Naples, Italy # Department of Food Science and Nutrition, Food Science and Nutrition Building, University of Minnesota, 1334 Eckles Avenue, St. Paul, Minnesota 55108, United States ABSTRACT: Thermal processing and Maillard reaction (MR) affect the nutritional and sensorial qualities of milk. In this paper an olive mill wastewater phenolic powder (OMW) was tested as a functional ingredient for inhibiting MR development in ultrahigh-temperature (UHT)-treated milk. OMW was added to milk at 0.1 and 0.05% w/v before UHT treatment, and the concentration of MR products was monitored to verify the effect of OMW phenols in controlling the MR. Results revealed that OMW is able to trap the reactive carbonyl species such as hydroxycarbonyls and dicarbonyls, which in turn led to the increase of Maillard-derived off-flavor development. The effect of OMW on the formation of Amadori products and N-ε-(carboxymethyl)lysine (CML) showed that oxidative cleavage, C2−C6 cyclization, and the consequent reactive carbonyl species formation were also inhibited by OMW. Data indicated that OMW is a functional ingredient able to control the MR and to improve the nutritional and sensorial attributes of milk. KEYWORDS: functional milk, olive oil phenols, Maillard reaction, reactive carbonyl species, olive mill wastewaters

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INTRODUCTION Thermal processing of foods guarantees milk safety and allows its long shelf life; however, it should be finely tuned to reach the equilibrium between the promotion of beneficial aspects and the reduction of thermal damages.1 The positive outcomes of food processing include the inactivation of foodborne pathogens or their toxins and the improvement of bioavailability, digestibility, and shelf life. Thermal processing may result in loss of texture and color, degradation of certain essential nutrients, formation of undesired compounds with negative sensorial properties, and a potentially toxic effect on human health.2 Many of the chemical modifications occurring during food thermal processing are connected to the Maillard reaction (MR). Maillard reaction products (MRPs) are formed by the reaction between reducing sugars and amino group counterparts;3 the formation of a glycosylamine is followed by the formation of two more stable intermediates: 1-amino-1-deoxy2-ketose, the Amadori rearrangement product (AP), and 2amino-2-deoxyaldose, the Heyns rearrangement product (HP).4 After this key step of the early stage of the MR a plethora of reactions can occur: sugar fragmentation and cyclization, Strecker’s aldehyde formation and degradation, retro-aldol condensation via the Namiki pathway, pyrolysis, oxidative cleavage, and polymerization. After the pivotal work by Hodges,5 70 years of research have well-defined the main pathways of the MR and identified several molecules that can act as a markers of MR development such as lysylpyrraline, carboxymethyl-lysine (CML), carboxyethyl-lysine (CEL), © 2014 American Chemical Society

pentosidine, furosine, hydroxymethylfurfural (HMF), and isomaltol.6,7 In milk products MR is not desired because of both sensory and nutritional reasons.8 Lactose-derived Amadori compounds are the main MR products in milk products, and their concentrations increased according to thermal treatment and water activity (pasteurization > ultrahigh temperature (UHT) > sterilization > milk powders) with a consequent blockage of the lysine residues and decrease of the nutritive value.9−11 Upon severe thermal conditions the breakdown of the Amadori products led to the formation of flavor compounds,12,13 antioxidant and pro-oxidant compounds,14−16 polymerization of proteins, and brown color development due to melanoidin generation.17−19 Recently, the issue of safety and the health consequences related to the intake of these dietary advanced glycation end products (dAGE) has been raised.20,21 Some papers highlighted their in vivo diabetogenic and nephrotoxic effects, and the term “glycotoxins” was even coined.22−24 Although no firm conclusions have been achieved about the dAGE physiological significance, studies to explore the correlation between biomarkers related to the thermal impact of milk process and nutritional physiological and toxicological outcomes are of great importance7,25,26 Received: Revised: Accepted: Published: 10092

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Merck (Darmstadt, Germany). The ion pairing agent perfluoropentanoic acid, trichloroacetic acid, hydrochloric acid (37%), sodium borohydride, sodium hydroxide, the analytical standards L-lysine hydrochloride, [4,4,5,5-d4]-L-lysine hydrochloride (d4-Lys), tyrosol (2-(4-hydroxyphenyl)ethanol, 98%), 3-hydroxytyrosol 98%, and verbascoside 98% along with glyoxal 40% solution in water, methylglyoxal 40% solution in water, and diacetyl (2,3-butanedione, 97%) as well as glycolaldehyde, acetoin, acetol, o-phenylenediamine (o-PD, 99.5%), and formic acid (MS grade 98%) were purchased from Sigma-Aldrich (St. Louis, MO, USA). Analytical standards N-ε-(2furoylmethyl)- L -lysine (furosine), N-ε-(carboxymethyl)- L -lysine (CML), and its respective deuterated standard N-ε-(carboxy[2H2]methyl)-L-lysine (d2-CML) were obtained from Polypeptide Laboratories (Strasbourg, France), whereas 3-deoxyglucosone, 13C4-acetoin, and 13C4-diacetyl were obtained from TRC (Toronto Research Chemicals, Ontario, Canada). Formulation of OMW. Olive oil mill wastewater polyphenol powders (OMW) were prepared from the water fraction resulting from olive oil production as follows. Olive water collected after olive paste centrifugation was treated with pectinases and fractionated by a filtration plant made up with three membranes at different cutoffs at 37 °C. Olive water was forced to pass through microfiltration (cutoff 25 kDa), ultrafiltration (cutoff 8 kDa), and nanofiltration (cutoff 0.3 kDa) membranes. At each stage a retentate containing the compounds not passing the membrane pores was collected. The ultrafiltration (UFR) retentate was concentrated by inverse osmosis (cutoff 0.1 kDa) up to 20% dry weight and spray-dried by adding maltodextrin and acacia fiber in a ratio 1:1 with the dry weight. A fine pale yellow powder with mild olive flavor was obtained and used in this study. OMW Characterization. The phenolic profile of OMW was characterized by reversed phase HPLC-UV−vis to quantify the phenylethanoids: hydroxytyrosol, tyrosol, and verbascoside. Briefly, 100 mg of powder was dissolved in 10 mL of water, and after the complete melting of the coating material (5 min, room temperature under continuous stirring), 1 mL was purified on a preactivated C-18 cartridge (1 cm3, 30 mg; Phenomenex, Torrance, CA, USA). Samples were eluted according to the method described by Kokkinidou and Peterson,49 and after drying, they were reconstituted in a mixture of water/methanol 95:5 (v/v); 20 μL was injected onto a Prodigy ODS3 250 mm × 4.6 reversed phase C-18 (Phenomenex). The UPLC system consisted of two binary pumps (LC-20A, Shimadzu, Kyoto, Japan) equipped with an UV−vis detector (SPD20A, Shimadzu). The mobile phases were water/0.1% formic acid (A) and methanol (B). Hydroxytyrosol, tyrosol, and verbascoside were separated according to the gradient 0 min, 5% B; 5 min, 5% B; 40 min, 70% B; 42 min, 70% B; 45 min, 5% B; 50 min, 5% B; and the typical retention times were 20, 23, and 28 min, respectively. The three analytes were quantified by the external standard technique and the results reported as milligrams per gram of powder. Laboratory-Scale UHT Milk Treatment. Raw milk (protein, 3.5%; fat, 1%) was obtained from a local market, and OMW was added to obtain final concentrations of 0.5 and 1 mg/mL. The three samples, one control and two samples with OMW, were homogenized, and after the complete dispersion of the powder (5 min, room temperature under continuous stirring) thermally treated in a laboratory-scale UHT milk system. It was constituted by three different tanks: two with oil, set at 180 and 140 °C, respectively, and another one with water at 6 °C. All of the samples were simultaneously treated, and one vial was used as reference. Along with 5 mL of milk, a thermocouple was inserted inside the reference headspace vial to control the time/ temperature profile of each set. The high temperature of the first batch allowed a rapid increase of the temperature in the vial; instead, the second tank stabilized the temperature at 140 °C for 5 s. At the end of the thermal process the samples were rapidly moved into the last tank where the cooling phase blocked the extent of the MR. Finally, as soon as the samples reached 15 °C, they were rapidly frozen in dry ice in ethanol and stored at −20 °C until the analysis. CML, Total Lysine, and Furosine Analysis. Total lysine and its derivatives N-ε-(carboxymethyl)lysine (CML) and N-ε-(2-furoylmethyl)-L-lysine (furosine) were analyzed according to the methods of

A characterization of food thermal damage can be achieved through the indirect measurement of the lysine APs such as lactulosyl-lysine or maltulosyl-lysine during acid hydrolysis by measuring furosine27,28 or bound HMF.29,30 More recently, some techniques allowed the direct measurement of the APs through LC/ESI-MS with or without labeled internal standard.4,31−33 Other two routinely indicators of thermal damage are CML and CEL, which can be analyzed by MALDI-TOF/ MS,34 LC-MS/MS after acidic hydrolysis stable isotope dilution assay,35,36 and GC-MS.37 This last technique is commonly used for the determination and accurate quantification of MR volatile compounds such as hydroxycarbonyls, glycolaldehyde, acetol, and acetoin, or off-flavor compounds such as methional and 2-acetyl-2-thiazoline.38−41 Last, but not least, a broad range of publications focuses on the determination of α-dicarbonyls by using different derivatizing agents.42,43 The control of the MR in food using functional ingredients can promote the formation of compounds having the desired color and flavor, and it can reduce the concentration of offflavors and potential toxic molecules. During the past years several approaches have been proposed to inhibit MR development in milk,44 specifically by using green tea extract or catechins.45,46 The mechanism behind the trapping activity of phenolic rings has been elucidated, and the chemical structure of the epicatechin−methylglyoxal adduct has been identified.47,48 Recently, response surface methodology has been used to investigate the dose−response relationship of a catechin, genistein, and diadzein mixture as a prethermal processing technique to reduce the formation of reactive carbonyl species (RCSs) such as glyoxal, methylglyoxal, and 3deoxyglucosone in ultrahigh-temperature (UHT) milk.49 Twenty compounds having an aromatic ring substituted with at least one hydroxyl group have been reacted with methylglyoxal: results about the trapping efficiency can be transferred to milk product to verify the possibility of producing new better quality milk beverages.50 Olive mill wastewater is a byproduct of the olive oil production process and represents an abundant source of phenolic compounds.51 olive mill wastewater typically contains 98% total phenols originally present in the olive, only a minor part being recovered in olive oil.52 olive mill wastewater contains >60 phenolic compounds, among which the most relevant are secoiridoid derivatives, such as hydroxytyrosol and the dialdehydic form of decarboxymethyl oleuropein aglycone along with tyrosol and verbascoside.53 The biological properties of its main components have been accurately reviewed;52 olive mill wastewater has been proposed for a wide range of applications including the production of nutraceuticals,54 the formulation of fish feed,55 and stabilization during lard production;56 however, its activity in preventing MR development in foods was never investigated. In this paper, the ability of an ingredient obtained from olive mill wastewater through ultrafiltration and successive spraydrying in controlling the MR in UHT milk was examined. Olive mill wastewater activity was tested in laboratory-scale UHT milk to verify its effectiveness in the reduction of early-stage MR products, such as free APs, protein-bound APs, and RCSs, in the reduction of off-flavor formation and in the inhibition of CML formation.

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MATERIAL AND METHODS

Chemicals. Acetonitrile, methanol, and water for solid phase extraction (SPE) and LC-MS/MS determination were obtained from 10093

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Milford, MA, USA). An Acquity UPLC 2.1 × 100 mm BEH Phenyl 1.7 μm column with a VanGuard 2.1 × 5 mm BEH Phenyl 1.7 μm precolumn was used for separation, and all experiments were performed in triplicate. Analytes were detected using electrospray positive ionization−multiple reaction monitoring (MRM) using methods previously developed and reported by Kokkinidou and Peterson and specifically designed to avoid quantitative interference from phenolic compounds and adducts.49 Quantification of Maillard Related Off-Flavor Volatiles. A dynamic headspace method was developed for the quantification of off-flavor markers, namely, 2-acetyl-2-thiazoline and methional. Analysis was performed using a 6890 GC equipped with a 5973 mass selective detector (Agilent Technologies), thermal desorption unit (TDU, Gerstel), PTV inlet (CIS 4, Gerstel), and MPS 2 (Gerstel). Briefly, 2 mL of nanopure water and 1 M sodium chloride were added to 5 mL of UHT milk (control and treatments) spiked with deuterated standards. Sample was then purged with nitrogen, drypurged to eliminate water, and then transferred to a thermal desorption unit. Measurements were performed 24 h after UHT processing using the analytical parameters summarized in Table 1.

Fenaille et al., Delatour et al., and Troise et al. with some modifications.35,36,57 Briefly, 100 μL of milk was mixed along with 0.45 mL of sodium borohydride (1 M in 0.1 N NaOH) and 0.5 mL of borate buffer (pH 9.2). The mixture was incubated for 4 h at room temperature to reduce the fructosyl-lysine in hexitol-lysine, and 1 mL of TCA (20% final concentradtion) was added to promote protein precipitation. Finally, 2 mL of 6 N HCl was added after careful removal of the supernatant. The mixture was incubated for 24 h at 110 °C in a forced-air circulating oven, and 400 μL was evaporated under a gentle flow of nitrogen. The samples were reconstituted in 380 μL of water, and 10 μL of the internal standard d2-CML and 10 μL of d4lysine were added to obtain a final concentration of 50 ng/mL for both standards. Samples were loaded onto equilibrated Oasis HLB 1 cm3 cartridges (Waters, Wexford, Ireland) and eluted according to the method previously described; finally, 5 μL was analyzed by ion pairing liquid chromatography coupled to MS/MS.57 Furosine, CML, lysine, and the respective internal standard separation was achieved on a reversed phase core−shell column (Kinetex C18, 2.1 mm × 100 mm, Phenomenex) with a C-18 precolumn (3.0 × 4.0 mm, Phenomenex) using the following mobile phases: (A) 5 mM perfluoropentanoic acid and (B) acetonitrile/5 mM perfluoropentanoic acid. Compounds were eluted at 200 μL/min through the following gradient of solvent B: 0 min, 10% B; 2 min, 10% B; 5 min, 70% B; 7 min, 70% B; 9 min, 90% B; 10 min, 90% B; 12 min, 10% B; 15 min, 10% B. With the abovedescribed chromatographic conditions, typical retention times for CML and d2-CML were 6.8 min; for d4-lysine and lysine, 7.03 min; and for furosine, 7.31 min. The MS/MS system was an API3000 (Applied Biosystems, Carlsbad, CA, USA); positive electrospray ionization was used for detection, and the source parameters were selected as follows: spray voltage, 5.0 kV; capillary temperature, 350 °C; dwell time, 100 ms. The chromatographic profile was recorded in multiple reaction monitoring mode, and the characteristic transitions were monitored to improve selectivity: for CML, furosine and lysine, the respective transitions of m/z 205−84.1, m/z 255.1−130.2, and m/ z 147.2−130.2 were used as quantifier, whereas m/z 205−130.2, m/z 255.1−84, and m/z 147.2−84.1 were used as qualifier. CML was quantified using d2-CML as internal standard (m/z 207−144.1 and 207−84 for quantification and confirmation, respectively), whereas for furosine and lysine, d4-lysine was used (m/z 151.2−134.1 and 151.1− 88 for quantification and confirmation, respectively). Free Amadori Products. For the detection of free Amadori products (APs), each milk sample was diluted 10 times with water and ultracentrifuged (14800 rpm, 10 min, 4 °C), and then the supernatants were accurately filtered (RC 0.45 μm, Phenomenex) and injected. For the chromatographic separation a reversed phase core−shell column (Kinetex C18, 2.1 mm × 100 mm, Phenomenex) with a C-18 precolumn (3.0 × 4.0 mm, Phenomenex) was used. The mobile phases consisted of 5 mM NFPA in water (solvent A) and 5 mM NFPA in acetonitrile (solvent B). The following gradient of solvent B was used: 0 min, 10% B; 2 min, 10% B; 5 min, 50% B; 7 min, 50% B; 9 min, 10% B; 12 min, 10% B; 15 min, 10% B. The flow rate was set to 200 μL/ min, and the injection volume was 5 μL. The U-HPLC was directly interfaced to an Exactive Orbitrap high-resolution mass spectrometer (HRMS) equipped with a heated electrospray interface (HESI). Mass spectrometer was operated in the full spectra positive ionization acquisition mode, in the mass range of m/z 65−500; the mass spectrometry parameters were set up according to Troise et al.58 Quantification of Reactive Carbonyl Species (RCSs). Methylglyoxal, glyoxal, 3-deoxyglucosone, and diacetyl (2,3-butanedione) as well as glycolaldehyde, acetoin, and acetol were quantified using the synthesized stable isotopes 13C4-acetoin and 13C4-diacetyl as internal standards. Each internal standard (0.5 mM) was added to 5 mL of milk, followed by 500 μL of 10% trichloroacetic acid. The samples were then vortexed and centrifuged at 3904g for 20 min at 4 °C (Beckman Coulter, Allegra X-22R), and the supernatant was collected. Solid phase extraction (SPE) method was used to isolate the compounds of interest and avoid interference from phenolic compounds and adducts. A derivatization method followed, and samples were analyzed using an Acquity UPLC system interfaced with a Quattro Premier XE micromass mass spectrometer (Waters Co.,

Table 1. Analysis Conditions Used for Identification and Quantification of Maillard-Related Off-Flavor Markers PTV

column oven MSD

chemical trap DHS unit

TDU unit

Analysis Conditions solvent vent (20 mL/min) at 7.1 psi solvent vent (0.5 min), 20 °C (0.5 min); 10 °C/s; 290 °C (4 min) DB5-MS, 30 m × 0.25 mm × 0.25 μm He, constant flow = 1 mL/min 40 °C (2 min); 4 °C/min; 160 °C 30 °C/min; 250 °C (5 min) SIM, 104 + 48 (methional), 107 + 51 (d3-methional), 129 (2-acetyl-2-thiazoline), 133 (d4-2-acetyl-2-thiazoline) Dynamic Headspace Component Tenax TA trap temperature: ambient, 40 °C sample incubation temperature (10 min) 1000 mL purge volume, 50 mL/min purge flow 320 mL dry volume, 40 mL/min dry flow solvent venting 20 °C (1 min); 720 °C/min; 290 °C (4 min)

Statistical Analysis. Each thermal treatment was repeated twice to improve the reliability of the laboratory-scale UHT system, whereas each sample was analyzed twice and injected two times. Results were reported as nanograms per milliliter of milk for RCSs, milligrams per 100 g of protein for furosine, lysine, and CML, and percent inhibition toward the control samples for free APs. Data were analyzed by ANOVA, and means were compared by Tukey’s test (α = 0.05) using XLStat statistical software (Addinsoft, New York, NY, USA).

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RESULTS AND DISCUSSION The use of a OMW ingredient obtained from ultrafiltered and spray-dried olive mill wastewater was evaluated for its ability to control the overall extent of the MR. The functional aspects of OMW were tested using a laboratory-scale UHT milk, and the selected outcomes were the MR aroma key odorants, the reduction of early-stage MRPs such as APs, the formation of protein-bound MRPs such as furosine and CML, and the ability to trap RCSs. The first part of the work involved the production of OMW by four subsequent steps: the starting material was made by the water resulting after oil separation, which was treated with pectinases and fractionated by three different membranes to obtain three different retentate fractions.59,60 The ultrafiltration 10094

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methional and 2-acetyl-2-thiazoline, commonly used as markers of off-flavor formation or aroma active compounds, were selected to verify the activity of OMW on this parameter. As shown in Figure 2 the concentration of methional was reduced from 4.08 ± 0.33 ng/mL for control UHT milk to 3.09 ± 0.26 and 2.15 ± 0.28 ng/mL for OMW 0.05% and OMW 0.1%, respectively. Furthermore, the concentration of 2-acetyl-2thiazoline was reduced from 0.87 ± 0.09 ng/mL for control UHT milk to 0.74 ± 0.11 and 0.48 ± 0.08 ng/mL for OMW 0.05% and OMW 0.1%, respectively. This means that compared to control UHT milk, OMW 0.05% reduced by 24.3 and 16.9% the concentrations of methional and 2-acetyl-2-thiazoline, respectively, albeit those reductions were not statistically significant. Increasing the OMW concentration to 0.1% reduced the concentrations of methional and 2-acetyl-2-thiazoline by 47.3 and 46.1%, respectively, when compared to control UHT milk. This reduction was significant, indicating a concentrationdependent effectiveness of the phenolic mixture in reducing offflavor generation during thermal processing. Data clearly showed that increasing the added OMW concentration prior to thermal processing can significantly decrease the concentration of off-flavor markers when compared to control UHT milk. These results were in line with those previously reported for the milk off-flavor and the potential role of added polyphenol.67−69 The trapping activity of OMW toward RCSs was evaluated by monitoring the concentrations of hydroxycarbonyl and dicarbonyl compounds in UHT milk with and without added OMW prior to thermal processing. The target RCSs monitored were glycoaldehyde, acetoin, and acetol for hydroxycarbonyls and glyoxal, methylglyoxal, 3-deoxyglucosone, and 2,3butanedione for α-dicarbonyls as they have been extensively studied for their contribution to AGE generation and carbonyl stress. Results are presented in Figures 3 and 4: the concentration of glycoaldehyde decreased from 246.03 ± 26.74 to 135.71 ± 30.63 and 105.36 ± 25.11 ng/mL for control UHT milk, OMW 0.05%, and OMW 0.1%, respectively, corresponding to reductions of 44.8 and 57.2% for samples containing OMW 0.05 and 0.1%. Similarly, OMW reduced the concentration of acetoin from 2293.73 ± 165.35 to 1897.91 ± 201.41 and 1321.86 ± 86.11 ng/mL for control UHT milk, OMW 0.05%, and OMW 0.1%, respectively, corresponding to reductions of 17.3 and 42.4% of acetoin for OMW 0.05 and 0.1% treatments. On the contrary, OMW did not show any reactivity toward acetol as no significant difference was observed between control UHT milk and OMW samples. These results can be explained on the basis of chemical reactivity as it follows the electophilicity of hydroxycarbonyl

Figure 1. Comparison between laboratory-scale UHT system and commercial indirect tubular UHT system. The holding time used was the same for direct UHT processing and UHT plaque sterilization.

retentate was concentrated by inverse osmosis up to 67% dry matter and spray-dried with acacia fiber and maltodextrin in a molar ratio of 1:1 to obtain a fine pale yellow powder.61 The phenolic profile of OMW was characterized by reversed phase UPLC-UV−vis to quantify the main constituents: hydroxytyrosol, tyrosol, and verbascoside. The concentrations of the three compounds in the OMW were 31 ± 0.2, 1.9 ± 0.1, and 2.8 ± 0.09 mg/g, respectively, in line with previous papers dealing with the composition of olive mill wastewater.51,53,62 Two different concentrations of OMW (0.05 and 0.1% w/v) were dissolved in raw cow’s milk, and their impact on thermal damage was investigated by monitoring several intermediates and end-products of MR. A laboratory-scale UHT treatment was developed for this purpose: the thermal profile of the treatment confirmed that the thermal load closely simulated those of a commercial indirect tubular UHT processing method as highlighted in Figure 1. In the system here developed the time/temperature profile was similar to the ones previously reported for commercial indirect tubular UHT processing, direct UHT processing, and plaque UHT sterilization.63,64 The sterilization factors were calculated according to Morales et al. using as reference temperature 127 °C and as z value 30 °C.65 They were 1.55 and 1.51 min for commercial UHT milk and laboratory-scale UHT milk, respectively. To compare the two concentrations of OMW, a control sample (without OMW) was simultaneously heated and several MRPs and RCSs were measured. In these conditions the final concentration of olive polyphenols reached a maximum of 36.1 mg/L without evident effects on milk sensory properties. Off-flavor formation in UHT milk was already investigated in different papers.12,66,67 According to the previous literature

Figure 2. Methional and 2-acetyl-2-thiazoline concentration in control UHT milk, milk with 0.05% OMW, and milk with 0.1% OMW. Different letters correspond to significant differences (Tukey test, α = 0.05). 10095

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Figure 3. Hydroxycarbonyl concentration in control UHT milk, milk with 0.05% OMW, and milk with 0.1% OMW. Different letters correspond to significant differences (Tukey test, α = 0.05). GA, glycoaldehyde.

Figure 4. α-Dicarbonyl concentration in control UHT milk, milk with 0.05% OMW, and milk with 0.1% OMW. Different letters correspond to significant differences (Tukey test, α = 0.05).

compounds and thus the reactivity of phenolic compounds toward trapping them: the electron-rich phenols present in OMW can easily react with electrophilic hydroxycarbonyl compounds due to the presence of a hydroxyl group in position α. Slight differences in the concentration of α-hydroxycarbonyls from previously reported papers can be ascribed to external factors such as microbial activity, starting material, and thermal treatments.69−71 The concentration of glyoxal was reduced from 2118.71 ± 113.94 ng/mL in control UHT milk to 1798.04 ± 218.49 and 1201.36 ± 136.73 ng/mL after the addition of OMW at 0.05 and 0.1%, respectively. This means reductions of 15.1 and

43.3% for glyoxal in samples with OMW 0.05 and 0.1% added, respectively. Methylglyoxal values were also reduced by 23.8 and 55.9% with OMW 0.05 and 0.1% addition, respectively. Both electrophilic dicarbonyls can give hydroxyalkylation of phenolic rings: Figure 4 suggests a higher activity of OMW toward methylglyoxal with respect to glyoxal, and this can be also due to the fact that the latter can polymerize in aqueous media, resulting in a lower affinity toward phenols.72 For both compounds the observed reductions were in line with those previously reported.49,50 The concentration of 2,3-butanedione was reduced from 11.79 ± 0.55 ng/mL for control UHT milk to 9.16 ± 1.04 and 5.98 ± 0.09 ng/mL for OMW 0.05% and 0.1%, respectively, 10096

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reduction of the AP formation and in turn of many MRPs via direct reaction with an amino group or via glyoxal trapping. As shown in Figure 5, the reduction of AP formation was particularly evident for hydrophobic glycated amino acids, such as isoleucine/leucine and glycine. This can be explained by the high concentration of these amino acids and their APs and by the lower reactivity relative to that of other amino acids toward reducing sugars. The best known compounds are the Amadori products N-ε-fructosyl-lysine and furosine. The effect of OMW on free N-ε-fructosyl-lysine formation was significant at both concentrations: 12.1 and 17.8% over the control sample for OMW 0.1% and OMW 0.05%, respectively. Finally the ability of OMW to reduce the formation of protein-bound CML and furosine was investigated. Results in Figure 6 show that after acidic hydrolysis the reduction of protein-bound MRPs was more pronounced for furosine; the reductions were 25.4 and 47.4% when OMW 0.05% and OMW 0.1% of phenolic powder were added, respectively. For CML the reductions were 11.2 and 16.2%, showing significant differences between the two phenolic powder concentrations and the control samples. Data on furosine showed that its concentration decreased from 10.962 ± 0.805 mg/100 g protein in the control UHT milk to 8.162 ± 0.794 and 5.761 ± 0.924 mg/100 g protein for OMW 0.05 and 0.1%, respectively. The differences between CML and furosine reduction can be tentatively explained in two ways. First, the two MRPs could follow two different pathways. Furosine is formed by cyclization through the C-6 hydroxyl group and dehydration reaction, and it reflects the protein-bound Amadori products of lysine, because the free N-ε-fructosyl-lysine is destroyed by acidic hydrolysis.4 CML can be formed by two mechanisms: the enediol form of the N-ε-fructosyl-lysine can undergo oxidative cleavage to produce CML and erythronic acid via free radical generation with simultaneous oxygen consumption, and glyoxal can easily block the amino group on the side chain via the Namiki pathway.74 Second, as shown in Figure 7, the reduction of both protein-bound and free MRPs can be associated not

Figure 5. Amadori product mean percent inhibition in control UHT milk, milk with 0.05% OMW, and milk with 0.1% OMW.

and 3-deoxyglucosone was modified only by the addition of the higher concentration of OMW as no significant difference was observed between control UHT milk and milk treated with OMW 0.05%. It can be hypothesized that the trapping activity toward 3-deoxyglucosone is affected by the partial charge on the oxygen of the carbon carbonyl in position 2, by the presence of other carbons that can stabilize the structure, and by steric hindrance. From this first set of experiments it can be concluded that OMW treatment was not very effective in trapping C6 sugar fragments, whereas a significative reactivity of phenolic compounds in OMW mixture was observed toward methylglyoxal, diacetyl, and glycoladehyde. All of the RCSs monitored are of interest not only for their contribution to MR pathways and carbonyl stress but also because they can contribute to the generation of off-flavor compounds; thus, their suppression can both directly and indirectly lead to a reduction in off-flavor generation. The effect of OMW was tested also in the reduction of free APs, which can be measured without protein hydrolysis, thanks to the relatively high content of free amino acids in milk.73 The formation of the AP was the central hub for the forthcoming steps of MR, so the presence of the phenolic rings favored the

Figure 6. CML, furosine, and total lysine concentrations in control UHT milk, milk with 0.05% OMW, and milk with 0.1% OMW. Different letters correspond to significant differences (Tukey test, α = 0.05). 10097

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Figure 7. Proposed mechanism of MRP reduction by phenolic compounds adapted from Totlani and Peterson,47 Estévez,76 and Guerra and Yaylayan.77 review on the beneficial aspects of food processing. Mol. Nutr. Food Res. 2010, 54, 1215−1247. (3) Maillard, L. C. Action of amino acids on sugars. Formation of melanoidins in a methodical way. Compt. Rend. 1912, 154, 66−68. (4) Yaylayan, V. A.; Huyghues-Despointes, A. Chemistry of Amadori rearrangement products: analysis, synthesis, kinetics, reactions, and spectroscopic properties. Crit. Rev. Food Sci. 1994, 34, 321−369. (5) Hodge, J. E. Dehydrated foods, chemistry of browning reactions in model systems. J. Agric. Food Chem. 1953, 1, 928−943. (6) Nursten, H. E. The Maillard Reaction: Chemistry, Biochemistry, and Implications; Royal Society of Chemistry: Cambridge, UK, 2005. (7) Pischetsrieder, M.; Henle, T. Glycation products in infant formulas: chemical, analytical and physiological aspects. Amino Acids 2012, 42, 1111−1118. (8) van Boekel, M. A. J. S. Effect of heating on Maillard reactions in milk. Food Chem. 1998, 62, 403−414. (9) Finot, A. P. Nutritional and metabolic aspects of protein modification during food processing. In Modification of Proteins: Food, Nutritional, and Pharmacological Aspects; Feeney, R. E., Whitaker, J. R., Eds.; American Chemical Society: Washington, DC, USA, 1982; Vol. 198. (10) Leclere, J.; Birlouez-Aragon, I. The fluorescence of advanced Maillard products is a good indicator of lysine damage during the Maillard reaction. J. Agric. Food Chem. 2001, 49, 4682−4687. (11) Monti, S. M.; Ritieni, A.; Graziani, G.; Randazzo, G.; Mannina, L.; Segre, A. L.; Fogliano, V. LC/MS analysis and antioxidative efficiency of Maillard reaction products from a lactose-lysine model system. J. Agric. Food Chem. 1999, 47, 1506−1513. (12) van Boekel, M. A. J. S. Formation of flavour compounds in the Maillard reaction. Biotechnol. Adv. 2006, 24, 230−233. (13) Zhang, Y. G.; Dorjpalam, B.; Ho, C. T. Contribution of peptides to volatile formation in the Maillard reaction of casein hydrolysate with glucose. J. Agric. Food Chem. 1992, 40, 2467−2471. (14) Calligaris, S.; Manzocco, L.; Anese, M.; Nicoli, M. C. Effect of heat-treatment on the antioxidant and pro-oxidant activity of milk. Int. Dairy J. 2004, 14, 421−427. (15) Morales, F. J.; Jimenez-Perez, S. Free radical scavenging capacity of Maillard reaction products as related to colour and fluorescence. Food Chem. 2001, 72, 119−125. (16) Jiang, Z. M.; Brodkorb, A. Structure and antioxidant activity of Maillard reaction products from α-lactalbumin and β-lactoglobulin with ribose in an aqueous model system. Food Chem. 2012, 133, 960− 968. (17) Chen, Y. J.; Liang, L.; Liu, X. M.; Labuza, T. P.; Zhou, P. Effect of fructose and glucose on glycation of β-lactoglobulin in an intermediate-moisture food model system: analysis by liquid chromatography-mass spectrometry (LC-MS) and data-independent acquisition LC-MS (LC-MSE). J. Agric. Food Chem. 2012, 60, 10674− 10682. (18) Rizzi, G. P. Chemical structure of colored Maillard reaction products. Food Rev. Int. 1997, 13, 1−28.

only with the reduction of the Amadori product of lysine and glucose but also with the above-described trapping activity. A trisubstituted phenolic ring with an ο-dihydroxy function can easily react with dicarbonyls by hydroxyalkylation and aromatic substitution reaction, thus showing trapping activity toward methylglyoxal and glyoxal.47,48,75 Moreover, in the presence of reactants such as ascorbic acid or iron, the phenolic ring can be oxidized to quinone, whose reaction with side chain of lysine and other amino group can lead to the formation of iminoquinone and iminophenol via Schiff bases as highlighted by Estévez76 and Guerra and Yaylayan.77 The results on CML and furosine fully confirmed those previously obtained by other groups.27,35,78 In conclusion, in this paper it was demonstrated that OMW besides its potential nutritional functionality could also help in the production of superior quality food and can provide an effective strategy in the control of the MR. The result was achieved on a broad range of MRPs that contributed to the final chemical composition of the UHT milk. Interestingly, these results were obtained in conditions not leading to easily detectable modifications of either physical properties (viscosity or color) or sensory properties (bitterness, astringency, olive flavor). However, the sensory acceptability of the addition of OMW should be further investigated.

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AUTHOR INFORMATION

Corresponding Author

*(V.F.) Phone: +31 (0)317 485171. Fax: +31 (0)317 485171. E-mail: [email protected]. Funding

This work was funded by the program PON01_ 02863 “Incapsulazione di principi attivi per il miglioramento di qualità e sicurezza degli alimenti” funded by the Italian Ministry of University and Scientific Research (MIUR). Notes

The authors declare no competing financial interest.

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ABBREVIATIONS USED MR, Maillard reaction; APs, Amadori products; RCSs, reactive carbonyl species; OMW, olive mill wastewater phenolic powder REFERENCES

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NOTE ADDED AFTER ASAP PUBLICATION This paper was published ASAP on October 3, 2014, with an error to Figure 4A. The corrected version was reposted on October 6, 2014.

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