Article pubs.acs.org/JAFC
Effects of Environmental pH on Antioxidant Interactions between Rosmarinic Acid and α‑Tocopherol in Oil-in-Water (O/W) Emulsions Ketinun Kittipongpittaya,‡ Atikorn Panya,*,† Natthaporn Phonsatta,† and Eric A. Decker§,⊥ †
Food Biotechnology Research Unit, National Center for Genetic Engineering and Biotechnology (BIOTEC), 113 Thailand Science Park, Phaholyothin Road, Khlong Nueng, Khlong Luang, Pathumthani 12120, Thailand ‡ Department of Agro-Industry Technology and Management, Faculty of Agro-Industry, King Mongkut’s University of Technology North Bangkok, Bangkok 10800, Thailand § Department of Food Science, Chenoweth Laboratory, University of Massachusetts, 100 Holdsworth Way, Amherst, Massachusetts 01003, United States ⊥ Bioactive Natural Products Research Group, Department of Biochemistry, Faculty of Science, King Abdulaziz University, P.O. Box 80203, Jeddah 21589, Saudi Arabia ABSTRACT: Antioxidant regeneration could be influenced by various factors such as antioxidant locations and pH conditions. The effects of environmental pH on the antioxidant interaction between rosmarinic acid and α-tocopherol in oil-in-water (O/W) emulsions were investigated. Results showed that the combined antioxidants at pH 7 exhibited the strongest synergistic antioxidant activity in comparison with the combinations at other pH conditions as indicated by the interaction index. A drop in pH from 7 to 3 resulted in a reduction in the synergistic effect. However, in the case of pH 3, an additive effect was obtained. Moreover, the effect of the pH on the regeneration of α-tocopherol by rosmarinic acid in heterogeneous Tween 20 solutions was studied using EPR spectrometer. The same was true for the regeneration efficiency, where the reaction at pH 7 exhibited the highest regeneration efficiency of 0.3 mol of α-tocopheroxyl radicals reduced/mol of phenolics. However, the study on depletions of rosmarinic acid and α-tocopherol revealed that the formation of caffeic acid, an oxidative degradation product of rosmarinic acid, could be involved in enhancing the antioxidant activity observed at pH 7 rather than the antioxidant regeneration. This study has highlighted that the importance of pH-dependent antioxidant interactions does not solely rely on antioxidant regeneration. In addition, the formation of other oxidative products from an antioxidant should be taken into account. KEYWORDS: antioxidant interaction, regeneration, rosmarinic acid, α-tocopherol
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INTRODUCTION Lipid oxidation, one of the major concerns for food industries, has deleterious effects not only on sensory quality but also on the nutrition and safety of food products. The most commonly used method to counteract lipid oxidation is an addition of several antioxidants. However, the numbers of approved antioxidants for foods are currently limited. Moreover, there are changes in consumer preferences and trends toward natural antioxidants in foods. Thus, under the current limitation, it is challenging to improve the performance of antioxidants to inhibit lipid oxidation in foods. One strategy is to enhance antioxidant efficiency by using a combination of antioxidants. The synergistic interactions of combined antioxidants could be produced via antioxidant regeneration by the recycling of a primary antioxidant with secondary antioxidant.1 From a thermodynamic point of view, a secondary antioxidant that has a reduction potential lower than the reduction potential of primary antioxidant is capable of donating electrons to oxidize a primary antioxidant, resulting in superior antioxidant activity.2 For example, radical transfer from ascorbic acid to α-tocopherol, one of the most effective synergistic interactions, has been widely reported in vivo and in vitro in both biological and food systems.3−6 Among other natural antioxidants, α-tocopherol, one of the highly potent primary antioxidants, is widely employed in the © 2016 American Chemical Society
food industry, not only because of its reduction potential (∼550 mV) but also because of its solubility in lipids. These allow α-tocopherol to localize at the lipid core and oil−water interface, which is able to effectively react with the lipid hydroperoxyl and/or the alkoxyl radicals formed by the metalcatalyzed decomposition of hydroperoxides,7 and also to be regenerated by other secondary antioxidants at the oil−water interfaces. In addition to ascorbic acid, the regeneration of αtocopherol by various phenolic antioxidants was reported in different environments.7−10 Our previous study on the regeneration of α-tocopherol by rosmarinic acid and its alkyl esters in oil-in-water (O/W) emulsions demonstrated that water-soluble rosmarinic acid exhibited the highest rate of α-tocopherol regeneration compared with its alkyl esters. Moreover, depending upon antioxidant locations in food systems, antioxidant interactions could result in various types of interactions such as synergistic, additive, and antagonistic effects.11 Interestingly, even though from the thermodynamic point of view the regeneration of αtocopherol by rosmarinic acid was an unfavorable chemical Received: Revised: Accepted: Published: 6575
June 15, 2016 July 28, 2016 August 5, 2016 August 5, 2016 DOI: 10.1021/acs.jafc.6b02700 J. Agric. Food Chem. 2016, 64, 6575−6583
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Journal of Agricultural and Food Chemistry
solution, 7.5 μL of 3.94 M ammonium thiocyanate, and 7.5 μL of ferrous iron solution (prepared by adding equal amounts of 0.132 M BaCl2 and 0.144 M FeSO4). After 20 min of incubation at room temperature, the absorbance was measured at 510 nm using a UV−vis spectrophotometer (Genesys 20, Thermo Spectronic). Lipid hydroperoxide concentrations were calculated on the basis of a standard curve prepared from cumene hydroperoxide. Measurements of Hexanal. Headspace hexanal was determined according to the method described by Panya and co-workers18 with some modifications using a Shimadzu GC-2014 gas chromatograph (GC) equipped with an AOC-5000 autoinjector (Shimadzu, Tokyo, Japan). A 50/30 μm divinylbenzene/carboxen/polydimethylsiloxane (DVB/carboxen/PDMS) stable flex solid phase microextraction (SPME) fiber (Supelco, Bellefonte, PA, USA) was inserted through the vial septum and exposed to the sample headspace for 8 min at 55 °C. The SPME fiber was desorbed at 250 °C for 3 min in the GC detector at a split ratio of 1:7. The chromatographic separation of volatile aldehydes was performed on a fused-silica capillary column (30 m × 0.32 mm i.d. × 1 μm) coated with 100% poly(dimethylsiloxane) (Equity-1, Supelco). The temperatures of the oven, injector, and flame ionization detector were 65, 250, and 250 °C, respectively. Sample run time was 10 min. Concentrations were calculated by using a standard curve made from the above emulsions containing known hexanal concentrations and 200 μM EDTA. Calculation of Antioxidant Interaction Indices of Rosmarinic Acid and α-Tocopherol Combinations. Interaction indices of rosmarinic acid with α-tocopherol were calculated on the basis of the oxidation lag times of lipid hydroperoxides and hexanal formation. Lag times were determined as the first data point that was statistically (p ≤ 0.05) greater than time zero. Briefly, the oxidation lag times of individual antioxidants were used to estimate the expected oxidation lag times of its combination. Interaction indices were calculated from the ratio between the obtained oxidation lag times of the combination and the expected oxidation lag time of the combination with the equation
reaction due to the reduction potential of rosmarinic acid being higher than α-tocopherol, the synergistic effect of such combination antioxidants still occurred. The results suggested that improving the antioxidant performance should not be solely focused on the regeneration. Apart from the regeneration and distribution of antioxidants, environmental pH conditions should also be evaluated in synergistic antioxidant studies. It was reported that electrochemical properties of antioxidants were pH dependent.12 For instance, reduction potentials of gallic acid in a buffer solution ranged from 190 to 520 mV at pH values from 7.0 to 2.0, respectively. In food emulsions, pH values could be widely varied. There have been several reports regarding the effect of pH on lipid oxidation and antioxidant activity in food emulsions.13−15 However, to our knowledge, the influence of pH on antioxidant interactions in food emulsion systems has not been investigated. Thus, this research aimed to study the effect of pH conditions on the antioxidant interactions between αtocopherol and rosmarinic acid in terms of α-tocopherol regeneration using an electron paramagnetic resonance (EPR) technique and their antioxidant performances in stripped soybean O/W emulsions.
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MATERIALS AND METHODS
Chemicals and Materials. Soybean oil was purchased from a local grocery store in Amherst, MA, USA. Ethylenediaminetetraacetic acid (EDTA) disodium salt was purchased from Chempure Ultra (Houston, TX, USA). Acetic acid, acetonitrile, methanol, and hydrochloric acid were obtained from Fisher Scientific (Pittsburgh, PA, USA). Rosmarinic acid, α-tocopherol, caffeic acid, FeSO4, Tween 20 (MW ≈ 1228), BaCl2, imidazole hydrochloride, sodium citrate, and 2,2,6,6-tetramethylpiperidinoxyl (TEMPO) radical were purchased from Sigma-Aldrich (St. Louis, MO, USA). Double-distilled and deionized water was used for the preparation of all solutions. Emulsion Preparation. Soybean oil was stripped to remove polar minor components (e.g., tocopherol, free fatty acid, mono- and diacylglycerol, phospholipid, hydroperoxides, etc.) according to the method of Waraho et al.16 The effectiveness of stripping was monitored by measuring the removal of tocopherols by HPLC.17 There was no tocopherol detected in the stripped oils. O/W emulsions were prepared using 1.0% (wt) stripped soybean oil in a 10 mM citrate−imidazole buffer solution (pH 7.0). Tween 20 was used as an emulsifier at a 1:10 emulsifier/oil ratio. Stripped soybean oil, Tween 20, and phosphate buffer were added to a beaker, and a coarse emulsion was made by blending with a hand-held homogenizer (M133/1281-0, Biospec Products, Inc., Bartlesville, OK, USA) for 2 min. The coarse emulsion was then homogenized with a microfluidizer (Microfluidics, Newton, MA, USA) at a pressure of 9 kbar for three passes. To prepare the O/W emulsions at pH 5.0 and 3.0, the prepared emulsion at pH 7.0 was then adjusted to the desired pH values using 1 M hydrochloric (HCl) solution. Rosmarinic acid and α-tocopherol in methanol were added to the emulsion at a final concentration of 30 μM and stirred for 1 h at room temperature. The solvent was removed by flushing with N2 gas. The emulsion without antioxidant was used as control sample. The emulsions (0.5 mL) were transferred into 10 mL GC vials and sealed with (tetrafluoroethylene) butyl rubber septa and then stored at 25 °C in the dark. Three vials of each treatment were taken every day to determine lipid hydroperoxide and hexanal formation. Measurements of Lipid Hydroperoxides. Lipid hydroperoxide formation in emulsions was determined according to the method described by Panya and co-workers18 with some modifications. Emulsion solutions (0.2 mL) were mixed with 1.5 mL of isooctane/ 2-propanol (3:1, v/v) and vortexed (10 s, three times). After centrifugation at 1000g for 2 min, 30 μL of the organic solvent phase was mixed with 1.5 mL of methanol/1-butanol (2:1, v/v)
interaction index =
observed lag time of the combination = expected lag time of the combination
{[lag time (control A + B) − lagtime (A + B)] /[lag time (control A) − lag time (A)] + [lag time (control B) − lag time (B)]}
where A and B represent α-tocopherol and rosmarinic acid, respectively. Controls of A, B, and A + B represent the lag time of individuals and combinations without added antioxidants. Interaction indices were expressed as synergistic (>1), additive (≈1), and antagonistic (1 (approximately 2−3), suggesting a synergistic effect. Moreover, such a synergistic effect was much higher in the combined antioxidants in O/W emulsion at pH 7 where the interaction index was around 5−7. This trend is in agreement with previous research showing that increasing 6579
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Figure 5. Regeneration efficiency of rosmarinic acid on α-tocopheroxyl radical in heterogeneous Tween 20 micelle solutions.
that the reduction potential peak and peak current of gallic acid were changed according to the pH changes. A decrease in the pH from pH 7 to 2 resulted in an increase in the reduction potential peak of gallic acid. Moreover, Mukai and co-workers demonstrated the effects of pH on rate constants of the reaction of flavonoids with the aroxyl radical (ArO•) in Triton X-100 micelles.27,28 It was found that the rate constants of flavonoids under neutral pH condition were much higher that the rate constants observed under acidic condition. It was suggested that one-step H atom transfer (HAT) and sequential proton-loss electron transfer (SPLET) are two main radical scavenging mechanisms in a polar medium.29,30 It was noted that partial ionization of antioxidants in ionizing solvents influenced by different pH conditions would prefer the SPLET process rather than HAT. Depletion of α-Tocopherol and Rosmarinic Acid during Oxidation of O/W Emulsion. Depending upon the oxidative hierarchy of antioxidants in a particular system, we hypothesized that α-tocopheroxyl radicals should be mainly formed because the majority of α-tocopherol (a lipid-soluble antioxidant) should be also mainly located in lipid oxidation sites such as the oil/water interface and oil phases. In this case, a sparing effect of α-tocopherol should be observed when another water-soluble antioxidant is combined. The regeneration of α-tocopherol by rosmarinic acid, as evidenced in the EPR study, could in part provide evidence of the synergistic activity observed in the oxidation study. However, the presence of oxidative degradation products of rosmarinic acid also might be a reason for the observation synergism. From LC-MS analysis in our previous study, we found that the antioxidant product obtained from rosmarinic acid in O/W emulsions was mainly caffeic acid, which formed via an oxidation breakdown of rosmarinate quinone.11 Caffeic acid served as an additional antioxidant that was responsible for the synergistic interaction between α-tocopherol and rosmarinic acid.11 However, to our knowledge, the effect of pH on the formation of caffeic acid from oxidation breakdown of rosmarinic acid has not been reported in the literature. Therefore, in the current study we aimed to investigate the influence of pH on the formation of caffeic acid along with the depletion of α-tocopherol and rosmarinic acid during storage of O/W emulsions at 25 °C using the HPLC technique. Interestingly, the patterns of antioxidant depletions were differently observed at various pH conditions. At pH 3, αtocopherol concentration gradually decreased over storage
respectively. Although rosmarinic acid is more water-soluble compared with α-tocopherol, our previous front-face fluorescence quenching study indicated that rosmarinic acid was able to interact with α-tocopherol with a relatively high quenching constant of 0.030 compared with other rosmarinate alkyl esters.11 This is partly due to the partitioning of αtocopherol by micelles formed by the excess surfactant to the aqueous phase where rosmarinic acid resides. The antioxidant interaction could be observed once they were in close proximity.11 Regeneration Efficiency of Rosmarinic Acid To Reduce α-Tocopheroxyl Radicals at Different pH Conditions. The regeneration efficiency of rosmarinic acid varied from 0.1 to 0.3 mol of α-tocopheroxyl radicals reduced/ mol of phenolics (Figure 5). Rosmarinic acid in O/W emulsion at pH 7 possessed the highest ability to donate electron toward α-tocopheroxyl radicals compared with rosmarinic acid in O/W emulsion at pH 5 and 3, respectively. The decreased regeneration efficiency of rosmarinic acid as a result of the pH decreases may be relevant to changes in the interaction index of the combined antioxidants. It should be noted that α-tocopheroxyl radicals were initially generated using DPPH radicals. The concentration of DPPH radicals used in the experiment was much lower than the αtocopherol content. The EPR spectra of DPPH radicals was not observed. Only the EPR spectra of α-tocopheroxyl radicals was found. This indicated that electrons were completely transferred from α-tocopherol to DPPH radicals. According to our previous research, the electron transfer from rosmarinic acid to α-tocopheroxyl radicals was thermodynamically unfavorable because the reduction potential of rosmarinic acid was found to be higher than that of αtocopherol.11 This suggested that even though the reaction was thermodynamically unfavorable, the regeneration still occurred. Laranjonha et al.26 speculated that the thermodynamically infeasible reactions of the regeneration of α-tocopherol by higher reduction potential antioxidants such as caffeic acid could actually occur due to solvation effects altering the reduction potential of the antioxidants. From this research, the result showed that the pH had dramatically affected the regeneration efficiency of rosmarinic acid to reduce α-tocopheroxyl radicals. There were several reports that the pH could strongly influence reduction potentials of antioxidants in polar protic solvents and scavenging mechanisms. Gunckel et al.12 had demonstrated 6580
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Figure 6. Depletion of rosmarinic acid and α-tocopherol and formation of caffeic acid in 1% stripped soybean oil/Tween 20 emulsions in 10 mM phosphate buffer, pH 3, at 25 °C in the presence of combined rosmarinic acid (30 μM) and α-tocopherol (30 μM). Data represent means (n = 3) ± standard deviations.
Figure 7. Depletion of rosmarinic acid and α-tocopherol and formation of caffeic acid in 1% stripped soybean oil/Tween 20 emulsions in 10 mM phosphate buffer, pH 5, at 25 °C in the presence of combined rosmarinic acid (30 μM) and α-tocopherol (30 μM). Data represent means (n = 3) ± standard deviations.
Figure 8. Depletion of rosmarinic acid α-tocopherol and formation of caffeic acid in 1% stripped soybean oil/Tween 20 emulsions in 10 mM phosphate buffer, pH 7, at 25 °C in the presence of combined rosmarinic acid (30 μM) and α-tocopherol (30 μM). Data represent means (n = 3) ± standard deviations.
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time, whereas rosmarinic acid was dramatically depleted at the early stage of storage (Figure 6). It was noted that caffeic acid concentration in O/W emulsion at pH 3 was relatively low at all times during storage. Thus, the lack of synergistic antioxidant effect observed at pH 3 could be due to not only the low regeneration efficiency of α-tocopherol and rosmarinic acid, as we presumed in the previous experiment, but also the quick loss of rosmarinic acid with the formation of a negligible level of caffeic acid at this pH. Unlike at pH 3, the concentration of caffeic acid dramatically increased, whereas that of α-tocopherol and rosmarinic acid instantly decreased at the early stage of study at pH 5 (Figure 7). Caffeic acid concentration rose to the maximum level on day 3, after which all antioxidants were depleted at similar rates. In contrast, rosmarinic acid was gradually depleted with a corresponding increase in caffeic acid at pH 7 (Figure 8). Once the amount of caffeic acid increased, the depletion rate of α-tocopherol began to slow, compared to that of the beginning stage of the oxidation. Then, the depletion rates of both α-tocopherol and caffeic acid were similar until the end of the experiment. This pattern is similar to what we observed in our previous study. It is noteworthy that rosmarinic acid was decomposed more rapidly than α-tocopherol at all pH values. This suggests that the increase in antioxidant activity of the combination of αtocopherol and rosmarinic acid was not due to the ability of αtocopherol to regenerate rosmarinic acid. On the other hand, this study reveals that the environmental pH plays an important role in the changes of antioxidant concentration and thus influences their antioxidant capacity. The formation of caffeic acid in combination with the relatively slow depletion rate of αtocopherol and rosmarinic acid provides a significant amount of α-tocopherol, rosmarinic acid, and caffeic acid remaining in the system; thus, they could work together and produce synergistic antioxidant activity at pH 7. In summary, this work draws attention to the influence of pH on antioxidant activity of individual rosmarinic acid and αtocopherol and their combination in stripped soybean O/W emulsion. The stronger synergistic antioxidant activity was found at pH 7 rather than at pH 5 or 3. Besides the rosmarinic acid regenerating α-tocopherol, the formation of caffeic acid plays an important role in increasing the antioxidant activity of the combination of rosmarinic acid and α-tocopherol in a pHdependent manner. This study provides important information for designing suitable antioxidant combinations to exert synergistic effects under a particular pH. The applications of synergistic antioxidant activity may be limited under low pH conditions such as acidic food emulsions.
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Article
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AUTHOR INFORMATION
Corresponding Author
*(A.P.) E-mail:
[email protected]. Phone: (+66) 21178031. Fax: (+66) 2117-8049. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS A.P. thanks Dr. Paul M. Lahti in the Chemistry Department, University of MassachusettsAmherst, for donating his valuable time to teach and guide me in the development of EPR techniques used in this research. 6582
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