- Email: [email protected]
Impact of global traditional seasonings on thermal Z-isomerization of (all-E)-lycopene in tomato puree
LWT - Food Science and Technology 116 (2019) 108565
Contents lists available at ScienceDirect
LWT - Food Science and Technology journal homepage: www.elsevier.com/locate/lwt
Short communication
Impact of global traditional seasonings on thermal Z-isomerization of (all-E)lycopene in tomato puree
T
Masaki Hondaa,∗, Hakuto Kageyamaa, Takashi Hibinoa, Yelin Zhangb, Kohei Ichihashic, Tetsuya Fukayac,d,∗∗, Motonobu Gotob a
Faculty of Science & Technology, Meijo University, Shiogamaguchi, Tempaku-ku, Nagoya, 468-8502, Japan Department of Materials Process Engineering, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8603, Japan c Innovation Division, Kagome Company, Limited, Nishitomiyama, Nasushiobara, 329-2762, Japan d Institutes of Innovation for Future Society, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8603, Japan b
A R T I C LE I N FO
A B S T R A C T
Keywords: Carotenoid E/Z-isomerization Allium species Capparis species Brassica species
The aim of this work was to investigate the effects of commercially available global traditional seasonings on the thermal Z-isomerization of tomato lycopene. On heating at 80 °C for 1 h, the total Z-isomer content of lycopene present in tomato puree containing 5% olive oil increased from 5.5% to 32.3%. When several seasonings were individually added to the mixture of tomato puree and 5% olive oil, the thermal Z-isomerization of lycopene was significantly increased. For instance, when 10% jerk sauce, tapenade, and Dijon mustard were added to the tomato mixture, the total Z-isomer content following heating increased to 58.7%, 50.2%, and 47.3%, respectively. The results indicated that certain food ingredients like escallion (Allium fistulosum L.), caper (Capparis spinosa L.), and mustard (Brassica juncea L.) have a Z-isomerization promoting effect. In addition, when heating was performed in the absence of those seasonings, the 13Z-isomer was mainly increased. On the other hand, in the presence of the above seasonings, the 5Z-isomer, which has higher functionality and storage stability than other Z-isomers, was significantly increased. Our finding that some seasonings have a Z-isomerization promoting effect is applicable to the production of tomato-based dishes containing higher proportions of lycopene Z-isomers, which have greater bioavailability.
1. Introduction Tomatoes are one of the most popular vegetables in the world and the daily consumption of tomato-rich foods offers multiple health benefits, such as decreased risk of several cancers and atherosclerosis (Capanoglu, Beekwilder, Boyacioglu, De Vos, & Hall, 2010). Lycopene (C40H56) is an acyclic carotenoid with 11 conjugated double bonds and plays a major role in the above health promoting benefits (Perveen et al., 2015). However, the bioavailability of carotenoids including lycopene is very low. For example, Ryan, O'Connell, O'Sullivan, Aherne, and O'Brien (2008) reported that the lycopene bioavailability of raw and cooked tomatoes was less than 10%, as evaluated using an in vitro digestion model. Recently, the use of Z-isomerization of carotenoids to increase their bioavailability has been studied extensively (Honda et al., 2019b). To illustrate, the oral administration of tangerine tomato juice (total Z-isomer content of lycopene: 94%) and red tomato juice (total Zisomer content of lycopene: 10%) in humans clearly showed that the
∗
lycopene bioavailability of the tangerine tomato juice was approximately 8.5 times higher than that of the red tomato juice (Cooperstone et al., 2015). Furthermore, many in vitro and in vivo studies have indicated that Z-isomers of lycopene were more bioavailable than the allE-isomer (Honda, Maeda, Fukaya, & Goto, 2018a; Honda et al., 2019b). Tomatoes are often used as a seasoning throughout the world, especially in Europe. In addition, tomatoes are highly compatible with other seasonings and are commonly combined, e.g., pizza sauce with tomatoes and tapenade, pasta sauce with tomatoes and colatura di alici, and dipping sauce with tomatoes and aioli, which have traditionally consumed in Europe. Recent researches indicated that certain food ingredients, such as onion (Allium cepa L.) (Rinaldi de Alvarenga et al., 2017; Honda et al., 2019; Yu, Gleize, Zhang, Caris-Veyrat, & Renard, 2019) and garlic (Allium sativum L.) (Honda et al., 2018b), enhance the thermal Z-isomerization of (all-E)-lycopene in tomatoes. However, the effects of the presence of different seasonings on the thermal Z-isomerization of lycopene have not been investigated. Here, we
Corresponding author. Faculty of Science & Technology, Meijo University, Shiogamaguchi, Tempaku-ku, Nagoya, 468-8502, Japan. Corresponding author. Innovation Division, Kagome Company, Limited, Nishitomiyama, Nasushiobara, 329-2762, Japan. E-mail addresses: [email protected] (M. Honda), [email protected] (T. Fukaya).
∗∗
https://doi.org/10.1016/j.lwt.2019.108565 Received 15 March 2019; Received in revised form 16 July 2019; Accepted 26 August 2019 Available online 27 August 2019 0023-6438/ © 2019 Elsevier Ltd. All rights reserved.
LWT - Food Science and Technology 116 (2019) 108565
M. Honda, et al.
investigated the effects of the addition of 35 commercially available global traditional seasonings on the thermal Z-isomerization of (all-E)lycopene in tomato puree. The results from the present study are expected to have significant implications in formulating tasty and healthy home cooking recipes using tomatoes with significantly higher lycopene bioavailability. 2. Materials and methods 2.1. Materials Tomato puree (lycopene content, 12 mg/100 g; total Z-isomer content, 5.5%) and pure olive oil were purchased from Kagome Co., Ltd. (Tokyo, Japan) and Nisshin Oillio Group, Ltd. (Tokyo, Japan), respectively. The seasonings used in this study are summarized in Supplementary Material Table S1 along with the main materials and suppliers. Analytical-grade acetone was obtained from Sigma-Aldrich Co., Ltd. (Poole, Dorset, UK) and HPLC-grade hexane was purchased from Kanto Chemical Co., Inc. (Tokyo, Japan). N,N-Diisopropylethylamine (DIPEA) was purchased from Tokyo Chemical Industry Co., Ltd. (Tokyo, Japan). 2.2. Thermal Z-isomerization of lycopene The samples were prepared so that the ratio of tomato puree, seasoning, and olive oil was 85:10:5 (w/w/w). As vegetable oils act as a mediator of the E/Z-isomerization reaction of carotenoids, 5% olive oil was added to the mixture (Honda et al., 2017b). The mixture was homogenized using a food processor and an approximately 20-g sample was transferred to a 100-mL screw-capped glass bottle. The headspace was then purged with nitrogen gas and the glass bottle was tightly capped immediately to minimize oxygen exposure and prevent water evaporation. Thermal treatment was carried out in a water bath at 80 °C for 1 h in the dark. 2.3. Lycopene extraction Fig. 1. Normal-phase HPLC chromatograms of (A) untreated tomato puree and thermally treated tomato puree (B) containing 5% olive oil, (C) 5% olive oil and 10% Dijon mustard, and (D) 5% olive oil and 10% jerk sauce at 80 °C for 1 h (5Z)-, (9Z)-, and (13Z)-Lycopene designated in the chromatograms were identified according to previous studies (Hengartner, U., Bernhard, K., Meyer, K., Englert, G., & Glinz, 1992; (Honda et al., 2015b) and 2017a). The peaks (1–15) were tentatively identified as shown in Table 1.
Lycopene isomers were extracted from thermally treated samples using acetone according to a previously described method (Honda et al., 2017b). In brief, 1 g of the sample was weighed and added to 30 mL of acetone. The extraction was performed by sonication for 10 min at < 10 °C to prevent E/Z-isomerization during the extraction. The extraction residue was removed by vacuum filtration using filter paper (number 2; Advantec Co., Ltd., Tokyo, Japan) and the residue was rinsed by acetone until the filtrate was colorless. Subsequently, the extraction solvent was evaporated under reduced pressure and the extract containing lycopene isomers was obtained. The extract was dissolved in 10 mL of hexane and filtered through a 0.22-μm PTFE membrane filter (Osaka Chemical Co., Ltd., Osaka, Japan) for analysis using normal-phase HPLC.
comparison of the HPLC retention time, visible spectral data (λmax), and Q-ratio which was defined as the height ratio of the Z-peak at approximately 360 nm to the main absorption peak. (Hengartner, U., Bernhard, K., Meyer, K., Englert, G., & Glinz, 1992; Honda et al., 2015b and 2017a).
2.4. HPLC analysis
2.5. Statistical analysis
The profile of lycopene isomers was analysed by normal-phase HPLC (Shimadzu Prominence system; Shimadzu Co., Ltd., Kyoto, Japan) with three Nucleosil 300-5 columns connected in tandem (3 × 250 mm length, 4.6 mm inner diameter, 5 mm particle size; GL Sciences Inc., Tokyo, Japan) and a diode array detector (SPD-M20A; Shimadzu Co., Ltd., Kyoto, Japan) according to a previous method (Honda et al., 2017b). Hexane containing 0.075% of DIPEA was used as the mobile phase. The column temperature and the mobile phase flow rate were maintained at 35 °C and 1 mL/min, respectively. Quantification of lycopene isomers in the samples was performed using peak area integration at 460 nm, where the differences in the molar extinction coefficients among the isomers are relatively small (Honda et al., 2015b and 2017a). The peaks of lycopene isomers were identified by
All data were collected in triplicate and are expressed as the mean ± standard deviation. For the studies of the effect of food ingredients and catalysts on the thermal Z-isomerization of lycopene, Dunnett's test (p < 0.05 or p < 0.001) was used to evaluate statistical significance compared to the control group using JMP software (version 14.1.0; SAS Institute Inc., Cary, NC, USA). 3. Results and discussion 3.1. Profile of lycopene isomers obtained after thermal treatment Representative chromatograms of the untreated and thermally treated samples are shown in Fig. 1. Before heating, most of the 2
LWT - Food Science and Technology 116 (2019) 108565
M. Honda, et al.
seasoning (control), the total Z-isomer content increased to 32.3%. On the other hand, some seasonings significantly enhanced Z-isomerization. For example, when pickled caper and kneaded wasabi were added, the total Z-isomer content was found to be more than twice that of the control. The results indicated that caper (Capparis spinosa L.) and wasabi (Eutrema japonicum) enhanced thermal Z-isomerization. Thus, the presence of caper in tapenade is probably a major reason for the enhanced thermal Z-isomerization. Caper has traditionally been used in tomato dishes; however, this is the first report that caper enhances the thermal Z-isomerization of lycopene. Thermal Z-isomerization was notably promoted when jerk sauce, which is traditionally used in Jamaica, was added. The main constituent of this seasoning is escallion (Allium fistulosum L.), which is likely to be one of the causal food ingredients having a Z-isomerization promoting effect of (all-E)-lycopene. Several studies also reported that the food ingredients of Allium plants, such as onion and garlic, enhance the thermal Z-isomerization of lycopene (Rinaldi de Alvarenga et al., 2017; Honda et al., 2018b; Yu et al., 2019). Furthermore, seasonings that contain garlic as the main ingredient, such as black bean sauce, aioli, and gochujang (Table S1), promoted the thermal Z-isomerization of (all-E)-lycopene. These results indicate that most Allium plants can enhance this process. Dijon mustard, which contains mustard (Brassica juncea L.) as the main component, exhibited the Z-isomerization promoting effect. A few studies have also indicated that Brassica plants, such as broccoli and cabbage, promote thermal isomerization of (all-E)-lycopene (Honda et al., 2019; Takemura, Honda, & Fukaya, 2019). In addition, some fish sauces such as nuocmam and shottsuru, yeast extracts such as marmite and vegemite, and cooking liquors such as mirin and red wine enhanced thermal Z-isomerization. The relative proportion of the 5Z-isomer, which is characterized by high functionality and storage stability among the Z-isomers (Honda et al., 2018a; Müller et al., 2011; Murakami et al., 2018), is shown in Fig. 2B. The 5Z-isomer content following heating was generally consistent with an increased degree of the total Z-isomer content. Of the 35 seasonings investigated, the top five that promoted 5Z-isomerization of lycopene following heating were as follows: jerk sauce (18.3%) > pickled caper (16.6%) > kneaded wasabi (16.2%) > tapenade (12.4%) > black bean sauce (10.7%) (Supplementary Table S2). From the above results, some causative components that promote thermal Z-isomerization can be deduced. We recently reported that
lycopene content in the sample was detected to be in all-E-configuration (Fig. 1A), whereas the percentage of Z-isomers increased following heating at 80 °C for 1 h (Fig. 1B), as described in previous reports (Honda et al., 2017b and 2017c). The addition of some seasonings such as jerk sauce and Dijon mustard clearly enhanced the thermal Z-isomerization and substantially changed the lycopene isomer profile in comparison to the profile in the absence of seasonings (see details in section 3.2.) (Fig. 1C and D). (13Z)-Lycopene was mainly increased in the thermally treated sample without seasoning (Fig. 1B, Table S2). On the other hand, the 9Z- and 5Z-isomers were predominantly increased in the presence of certain seasonings (Fig. 1C and D, Table S2). Several studies have shown that, among lycopene isomers, (5Z)-lycopene is likely to have higher bioavailability and antioxidant activity than the other isomers (Honda et al., 2018a; Müller et al., 2011). Moreover, the 5Z-isomer has the highest storage stability of the mono-Z-isomers and its stability is similar to the all-E-isomer (Honda et al., 2017a; Murakami et al., 2018). Namely, (13Z)- and (9Z)-lycopene are isomerized to the all-E-isomer during storage under the influence of heat and light, whereas (5Z)-lycopene is stable against heat and light (Murakami et al., 2018). To expand product storage life is essential from an industrial viewpoint and thus, it is very important to clarify the seasoning(s) that can increase the 5Z-isomer. Since (5Z)-lycopene has the highest activation energy (Ea) from the all-E-isomer to the mono-Zisomers (Honda et al., 2017a), its production from the all-E-isomer requires significant thermal energy. However, the addition of several seasonings, such as jerk sauce, resulted in the 5Z-isomer being the predominant Z-isomer produced (Fig. 1 D). This suggests that such seasonings are likely to contain catalysts like iron(III) chloride and diallyl disulfide, which lower the activation energy (Ea) for the production of (5Z)-lycopene from the all-E-isomer (Honda et al., 2018b; Honda, Kawana, Takehara, & Inoue, 2015a; Yu et al., 2019). 3.2. Effect of seasonings on thermal Z-isomerization of tomato lycopene The impact of 35 commercially available global traditional seasonings (Table S1) on thermal Z-isomerization of (all-E)-lycopene contained in tomato puree was investigated. After heating at 80 °C for 1 h, lycopene was not decomposed to any significant extent. (Table S2). The total Z-isomer content of lycopene following heating is shown in Fig. 2A. When the thermal treatment was performed in the absence of
Table 1 Tentative identification of lycopene isomers using normal-phase high-performance liquid chromatography with diode array detector.a Peak
Lycopene isomerb
λmax (nm)
Q-Ratio
Observed 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
(9Z,13′Z) ULZ (9Z, 9′Z) ULZ ULZ (5Z,13′Z) (13Z) ULZ ULZ ULZ ULZ (5Z,9′Z) ULZ (9Z) (5Z,9Z,5′Z) (5Z,9Z) (5Z,5′Z) (all-E) (5Z)
360, 361, 360, 360, 360, 360, 360, 360, 360, 360, 360, 361, 360, 360, 360, 360, 442, 444, 444,
432, 432, 432, 440, 432, 440, 439, 441, 432, 432, 432, 439, 432, 439, 442, 438, 469, 470, 470,
Reported 458, 457, 461, 465, 457, 465, 464, 467, 457, 457, 457, 464, 452, 463, 463, 463, 502 501 501
488 484 488 496 484 497 496 498 484 484 484 495 487 495 496 495
361, – 361, – – 361, 361, – – – – 361, – 361, 361, 361, 443, 444, 444,
b
434, 459, 489 435, 460, 491
439, 465, 497 437, 463, 494
442, 467, 497 442, 442, 440, 470, 471, 471,
467, 497 467, 497 460, 497 501 502 502
Observed
Reportedb
0.29 0.24 0.11 0.42 0.25 0.43 0.44 0.32 23.7 0.11 0.24 0.13 0.26 0.14 0.12 0.12 ND ND ND
0.31 – 0.11 – – 0.56 0.59 – – – – 0.13 – 0.13 0.13 0.13 ND ND ND
a Values and peak designations were obtained from the chromatograms in Fig. 1. ULZ, unidentified lycopene Z-isomer. –, not assigned. ND, not detected substantially. b Tentatively assigned in the literatures (Hengartner, U., Bernhard, K., Meyer, K., Englert, G., & Glinz, 1992; Honda et al., 2015b and 2017a).
3
LWT - Food Science and Technology 116 (2019) 108565
M. Honda, et al.
Fig. 2. Effect of addition of seasonings on the thermal Z-isomerization of lycopene contained in tomato puree. (A) Effect on total Z-isomer content, (B) effect on 5Zisomer content. Error bars show standard deviation (n = 3). * and ** indicate statistically significant differences (Dunnett's test) from the control group at p < 0.05 and p < 0.001, respectively.
dissolved in ethanol (0.6 mg/L at 20 °C; Murakami et al., 2017). Our findings on the effect of the addition of seasonings on the thermal Zisomerization of lycopene are important, not only for the food and beverage manufacturing industries, but also for developing more nutritious home cooking recipes.
diallyl disulfide, which is frequently found in plants of the Allium species, enhanced thermal Z-isomerization of (all-E)-lycopene (Honda et al., 2018b). Thus, it is thought that polysulfides would be a causative component of the seasonings containing escallion (Allium fistulosum L.) and garlic (Allium sativum L.), e.g., jerk sauce and aioli. Moreover, disulfide compounds are produced by the Maillard reaction (Xu, Liu, Zhao, & Gao, 2008). Since the Maillard reaction occurs during the fermentation of fish sauce and yeast extract, the causative components of those seasonings are suggested to be the disulfide compounds. In fact, several studies have reported that fish sauce (nam-pla) and yeast extract contain diallyl disulphide (Lin et al., 2014; Yongsawatdigul, Rodtong, & Raksakulthai, 2007). This study revealed that caper, wasabi, and mustard might promote the Z-isomerization reaction. Our recent study shows that isothiocyanates promote the thermal Z-isomerization of (allE)-lycopene (Honda et al., 2019), and these food ingredients commonly contain considerable quantities of isothiocyanates such as allyl isothiocyanate and benzyl isothiocyanate (Jordt et al., 2004). Thus, it is proposed that the presence of isothiocyanates accounts for the ability of pickled caper, kneaded wasabi, tapenade, and Dijon mustard to promote the thermal Z-isomerization of (all-E)-lycopene. Cooking alcohols also promoted this process, with ethanol being one of the causative components. Several studies have reported that the presence of a mediator(s), i.e., organic solvents and oils, enhanced thermal Z-isomerization of (all-E)-carotenoids (Honda et al., 2015b and 2017b). Namely, E/Z-isomerization reaction of carotenoids is more facile in a dissolved state. Although the solubility is low, (all-E)-lycopene can be
4. Conclusions The effect of 35 global traditional seasonings on thermal Z-isomerization of (all-E)-lycopene contained in tomato puree was investigated. Several seasonings, e.g., jerk sauce, tapenade, aioli, and Dijon mustard, notably promoted the Z-isomerization. We attribute this to the presence of causal food ingredients such as escallion (Allium fistulosum L.), caper (Capparis spinosa L.), garlic (Allium sativum L.), and mustard (Brassica juncea L.), which contain disulfide compounds and isothiocyanates that lower the activation energy, and therefore, enhance the Z-isomerization process. These findings are important, not only for the production of high value-added processed tomato products, but also for optimal nutrition when cooking at home. Acknowledgements This work was partly supported by JSPS KAKENHI Grant Number 19K15779and the Tatematsu Foundation, and the Hokuto Foundation for Bioscience. The authors are grateful to T. Kumagai, C. Kitamura, Y. Inoue, and M. Takehara (The University of Shiga Prefecture), and H. 4
LWT - Food Science and Technology 116 (2019) 108565
M. Honda, et al.
Ueda, T. Higashiura, and R. Takemura (Kagome Co., Ltd.) for their kind help and constructive suggestions.
Microwave-accelerated Z-isomerization of (all-E)-lycopene in tomato oleoresin and enhancement of the conversion by vegetable oils containing disulfide compounds. European Journal of Lipid Science and Technology, 120(1–9), 1800060. Honda, M., Takahashi, N., Kuwa, T., Takehara, M., Inoue, Y., & Kumagai, T. (2015b). Spectral characterisation of Z-isomers of lycopene formed during heat treatment and solvent effects on the E/Z isomerisation process. Food Chemistry, 171, 323–329. Honda, M., Watanabe, Y., Murakami, K., Takemura, R., Fukaya, T., Kanda, H., et al. (2017c). Thermal isomerization pre-treatment to improve lycopene extraction from tomato pulp. LWT-Food Science and Technology, 86, 69–75. Jordt, S. E., Bautista, D. M., Chuang, H. H., McKemy, D. D., Zygmunt, P. M., Högestätt, E. D., et al. (2004). Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature, 427, 260–265. Lin, M., Liu, X., Xu, Q., Song, H., Li, P., & Yao, J. (2014). Aroma‐active components of yeast extract pastes with a basic and characteristic meaty flavour. Journal of the Science of Food and Agriculture, 94, 882–889. Murakami, K., Honda, M., Takemura, R., Fukaya, T., Kanda, H., & Goto, M. (2018). Effect of thermal treatment and light irradiation on the stability of lycopene with high Zisomers content. Food Chemistry, 250, 253–258. Murakami, K., Honda, M., Takemura, R., Fukaya, T., Kubota, M., Kanda, H., et al. (2017). The thermal Z-isomerization-induced change in solubility and physical properties of (all-E)-lycopene. Biochemical and Biophysical Research Communications, 491, 317–322. Müller, L., Goupy, P., Fröhlich, K., Dangles, O., Caris-Veyrat, C., & Böhm, V. (2011). Comparative study on antioxidant activity of lycopene (Z)-isomers in different assays. Journal of Agricultural and Food Chemistry, 59, 4504–4511. Perveen, R., Suleria, H. A. R., Anjum, F. M., Butt, M. S., Pasha, I., & Ahmad, S. (2015). Tomato (Solanum lycopersicum) carotenoids and lycopenes chemistry; metabolism, absorption, nutrition, and allied health claims—a comprehensive review. Critical Reviews in Food Science and Nutrition, 55, 919–929. Rinaldi de Alvarenga, J. F., Tran, C., Hurtado-Barroso, S., Martinez-Huélamo, M., Illan, M., & Lamuela-Raventos, R. M. (2017). Home cooking and ingredient synergism improve lycopene isomer production in Sofrito. Food Research International, 99, 851–861. Ryan, L., O'Connell, O., O'Sullivan, L., Aherne, S. A., & O'Brien, N. M. (2008). Micellarisation of carotenoids from raw and cooked vegetables. Plant Foods for Human Nutrition, 63, 127–133. Takemura, R., Honda, M., & Fukaya, T. (2019). Enhanced cis-isomerization of (all-trans)lycopene in tomato products with via specific vegetables in home cooking. Journal of Cookery Science of Japan, 52, 57–66. Xu, H., Liu, X., Zhao, J., & Gao, Y. (2008). Effects of ribose to cysteine ratios on the formation of volatile compounds from the Maillard reaction in supercritical carbon dioxide. Food Research International, 41, 730–737. Yongsawatdigul, J., Rodtong, S., & Raksakulthai, N. (2007). Acceleration of Thai fish sauce fermentation using proteinases and bacterial starter cultures. Journal of Food Science, 72, M382–M390. Yu, J., Gleize, B., Zhang, L., Caris-Veyrat, C., & Renard, C. M. (2019). Heating tomato puree in the presence of lipids and onion: The impact of onion on lycopene isomerization. Food Chemistry, 296, 9–16.
Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.lwt.2019.108565. References Capanoglu, E., Beekwilder, J., Boyacioglu, D., De Vos, R. C., & Hall, R. D. (2010). The effect of industrial food processing on potentially health-beneficial tomato antioxidants. Critical Reviews in Food Science and Nutrition, 50, 919–930. Cooperstone, J. L., Ralston, R. A., Riedl, K. M., Haufe, T. C., Schweiggert, R. M., King, S. A., et al. (2015). Enhanced bioavailability of lycopene when consumed as cis-isomers from tangerine compared to red tomato juice, a randomized, cross-over clinical trial. Molecular Nutrition & Food Research, 59, 658–669. Hengartner, U., Bernhard, K., Meyer, K., Englert, G., & Glinz, E. (1992). Synthesis, isolation, and NMR-spectroscopic characterization of fourteen (Z)-isomers of lycopene and of some acetylenic didehydro- and tetradehydrolycopenes. Helvetica Chimica Acta, 75, 1848–1865. Honda, M., Kageyama, H., Hibino, T., Takemura, R., Goto, M., & Fukaya, T. (2019a). Enhanced Z-isomerization of tomato lycopene through the optimal combination of food ingredients. Scientific Reports, 9(1–7), 7979. Honda, M., Kageyama, H., Hibino, T., Zhang, Y., Wahyudiono Kanda, H., et al. (2019b). Improved carotenoid processing with sustainable solvents utilizing Z-isomerizationinduced alteration in physicochemical properties: A review and future directions. Molecules, 24(1–19), 2149. Honda, M., Kawana, T., Takehara, M., & Inoue, Y. (2015a). Enhanced E/Z isomerization of (all-E)-lycopene by employing iron(III) chloride as a catalyst. Journal of Food Science, 80, C1453–C1459. Honda, M., Kudo, T., Kuwa, T., Higashiura, T., Fukaya, T., Inoue, Y., et al. (2017a). Isolation and spectral characterization of thermally generated multi-Z-isomers of lycopene and the theoretically preferred pathway to di-Z-isomers. Bioscience, Biotechnology, and Biochemistry, 81, 365–371. Honda, M., Maeda, H., Fukaya, T., & Goto, M. (2018a). Effects of Z-isomerization on the bioavailability and functionality of carotenoids: A review. In L. Q. Zepla, E. JacobLopes, & V. V. De Rosso (Eds.). Progress in carotenoid research (pp. 139–159). London: IntechOpen. Honda, M., Murakami, K., Watanabe, Y., Higashiura, T., Fukaya, T., Kanda, H., et al. (2017b). The E/Z isomer ratio of lycopene in foods and effect of heating with edible oils and fats on isomerization of (all-E)-lycopene. European Journal of Lipid Science and Technology, 119(1–9), 1600389. Honda, M., Sato, H., Takehara, M., Inoue, Y., Kitamura, C., Takemura, R., et al. (2018b).
5
Contents lists available at ScienceDirect
LWT - Food Science and Technology journal homepage: www.elsevier.com/locate/lwt
Short communication
Impact of global traditional seasonings on thermal Z-isomerization of (all-E)lycopene in tomato puree
T
Masaki Hondaa,∗, Hakuto Kageyamaa, Takashi Hibinoa, Yelin Zhangb, Kohei Ichihashic, Tetsuya Fukayac,d,∗∗, Motonobu Gotob a
Faculty of Science & Technology, Meijo University, Shiogamaguchi, Tempaku-ku, Nagoya, 468-8502, Japan Department of Materials Process Engineering, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8603, Japan c Innovation Division, Kagome Company, Limited, Nishitomiyama, Nasushiobara, 329-2762, Japan d Institutes of Innovation for Future Society, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8603, Japan b
A R T I C LE I N FO
A B S T R A C T
Keywords: Carotenoid E/Z-isomerization Allium species Capparis species Brassica species
The aim of this work was to investigate the effects of commercially available global traditional seasonings on the thermal Z-isomerization of tomato lycopene. On heating at 80 °C for 1 h, the total Z-isomer content of lycopene present in tomato puree containing 5% olive oil increased from 5.5% to 32.3%. When several seasonings were individually added to the mixture of tomato puree and 5% olive oil, the thermal Z-isomerization of lycopene was significantly increased. For instance, when 10% jerk sauce, tapenade, and Dijon mustard were added to the tomato mixture, the total Z-isomer content following heating increased to 58.7%, 50.2%, and 47.3%, respectively. The results indicated that certain food ingredients like escallion (Allium fistulosum L.), caper (Capparis spinosa L.), and mustard (Brassica juncea L.) have a Z-isomerization promoting effect. In addition, when heating was performed in the absence of those seasonings, the 13Z-isomer was mainly increased. On the other hand, in the presence of the above seasonings, the 5Z-isomer, which has higher functionality and storage stability than other Z-isomers, was significantly increased. Our finding that some seasonings have a Z-isomerization promoting effect is applicable to the production of tomato-based dishes containing higher proportions of lycopene Z-isomers, which have greater bioavailability.
1. Introduction Tomatoes are one of the most popular vegetables in the world and the daily consumption of tomato-rich foods offers multiple health benefits, such as decreased risk of several cancers and atherosclerosis (Capanoglu, Beekwilder, Boyacioglu, De Vos, & Hall, 2010). Lycopene (C40H56) is an acyclic carotenoid with 11 conjugated double bonds and plays a major role in the above health promoting benefits (Perveen et al., 2015). However, the bioavailability of carotenoids including lycopene is very low. For example, Ryan, O'Connell, O'Sullivan, Aherne, and O'Brien (2008) reported that the lycopene bioavailability of raw and cooked tomatoes was less than 10%, as evaluated using an in vitro digestion model. Recently, the use of Z-isomerization of carotenoids to increase their bioavailability has been studied extensively (Honda et al., 2019b). To illustrate, the oral administration of tangerine tomato juice (total Z-isomer content of lycopene: 94%) and red tomato juice (total Zisomer content of lycopene: 10%) in humans clearly showed that the
∗
lycopene bioavailability of the tangerine tomato juice was approximately 8.5 times higher than that of the red tomato juice (Cooperstone et al., 2015). Furthermore, many in vitro and in vivo studies have indicated that Z-isomers of lycopene were more bioavailable than the allE-isomer (Honda, Maeda, Fukaya, & Goto, 2018a; Honda et al., 2019b). Tomatoes are often used as a seasoning throughout the world, especially in Europe. In addition, tomatoes are highly compatible with other seasonings and are commonly combined, e.g., pizza sauce with tomatoes and tapenade, pasta sauce with tomatoes and colatura di alici, and dipping sauce with tomatoes and aioli, which have traditionally consumed in Europe. Recent researches indicated that certain food ingredients, such as onion (Allium cepa L.) (Rinaldi de Alvarenga et al., 2017; Honda et al., 2019; Yu, Gleize, Zhang, Caris-Veyrat, & Renard, 2019) and garlic (Allium sativum L.) (Honda et al., 2018b), enhance the thermal Z-isomerization of (all-E)-lycopene in tomatoes. However, the effects of the presence of different seasonings on the thermal Z-isomerization of lycopene have not been investigated. Here, we
Corresponding author. Faculty of Science & Technology, Meijo University, Shiogamaguchi, Tempaku-ku, Nagoya, 468-8502, Japan. Corresponding author. Innovation Division, Kagome Company, Limited, Nishitomiyama, Nasushiobara, 329-2762, Japan. E-mail addresses: [email protected] (M. Honda), [email protected] (T. Fukaya).
∗∗
https://doi.org/10.1016/j.lwt.2019.108565 Received 15 March 2019; Received in revised form 16 July 2019; Accepted 26 August 2019 Available online 27 August 2019 0023-6438/ © 2019 Elsevier Ltd. All rights reserved.
LWT - Food Science and Technology 116 (2019) 108565
M. Honda, et al.
investigated the effects of the addition of 35 commercially available global traditional seasonings on the thermal Z-isomerization of (all-E)lycopene in tomato puree. The results from the present study are expected to have significant implications in formulating tasty and healthy home cooking recipes using tomatoes with significantly higher lycopene bioavailability. 2. Materials and methods 2.1. Materials Tomato puree (lycopene content, 12 mg/100 g; total Z-isomer content, 5.5%) and pure olive oil were purchased from Kagome Co., Ltd. (Tokyo, Japan) and Nisshin Oillio Group, Ltd. (Tokyo, Japan), respectively. The seasonings used in this study are summarized in Supplementary Material Table S1 along with the main materials and suppliers. Analytical-grade acetone was obtained from Sigma-Aldrich Co., Ltd. (Poole, Dorset, UK) and HPLC-grade hexane was purchased from Kanto Chemical Co., Inc. (Tokyo, Japan). N,N-Diisopropylethylamine (DIPEA) was purchased from Tokyo Chemical Industry Co., Ltd. (Tokyo, Japan). 2.2. Thermal Z-isomerization of lycopene The samples were prepared so that the ratio of tomato puree, seasoning, and olive oil was 85:10:5 (w/w/w). As vegetable oils act as a mediator of the E/Z-isomerization reaction of carotenoids, 5% olive oil was added to the mixture (Honda et al., 2017b). The mixture was homogenized using a food processor and an approximately 20-g sample was transferred to a 100-mL screw-capped glass bottle. The headspace was then purged with nitrogen gas and the glass bottle was tightly capped immediately to minimize oxygen exposure and prevent water evaporation. Thermal treatment was carried out in a water bath at 80 °C for 1 h in the dark. 2.3. Lycopene extraction Fig. 1. Normal-phase HPLC chromatograms of (A) untreated tomato puree and thermally treated tomato puree (B) containing 5% olive oil, (C) 5% olive oil and 10% Dijon mustard, and (D) 5% olive oil and 10% jerk sauce at 80 °C for 1 h (5Z)-, (9Z)-, and (13Z)-Lycopene designated in the chromatograms were identified according to previous studies (Hengartner, U., Bernhard, K., Meyer, K., Englert, G., & Glinz, 1992; (Honda et al., 2015b) and 2017a). The peaks (1–15) were tentatively identified as shown in Table 1.
Lycopene isomers were extracted from thermally treated samples using acetone according to a previously described method (Honda et al., 2017b). In brief, 1 g of the sample was weighed and added to 30 mL of acetone. The extraction was performed by sonication for 10 min at < 10 °C to prevent E/Z-isomerization during the extraction. The extraction residue was removed by vacuum filtration using filter paper (number 2; Advantec Co., Ltd., Tokyo, Japan) and the residue was rinsed by acetone until the filtrate was colorless. Subsequently, the extraction solvent was evaporated under reduced pressure and the extract containing lycopene isomers was obtained. The extract was dissolved in 10 mL of hexane and filtered through a 0.22-μm PTFE membrane filter (Osaka Chemical Co., Ltd., Osaka, Japan) for analysis using normal-phase HPLC.
comparison of the HPLC retention time, visible spectral data (λmax), and Q-ratio which was defined as the height ratio of the Z-peak at approximately 360 nm to the main absorption peak. (Hengartner, U., Bernhard, K., Meyer, K., Englert, G., & Glinz, 1992; Honda et al., 2015b and 2017a).
2.4. HPLC analysis
2.5. Statistical analysis
The profile of lycopene isomers was analysed by normal-phase HPLC (Shimadzu Prominence system; Shimadzu Co., Ltd., Kyoto, Japan) with three Nucleosil 300-5 columns connected in tandem (3 × 250 mm length, 4.6 mm inner diameter, 5 mm particle size; GL Sciences Inc., Tokyo, Japan) and a diode array detector (SPD-M20A; Shimadzu Co., Ltd., Kyoto, Japan) according to a previous method (Honda et al., 2017b). Hexane containing 0.075% of DIPEA was used as the mobile phase. The column temperature and the mobile phase flow rate were maintained at 35 °C and 1 mL/min, respectively. Quantification of lycopene isomers in the samples was performed using peak area integration at 460 nm, where the differences in the molar extinction coefficients among the isomers are relatively small (Honda et al., 2015b and 2017a). The peaks of lycopene isomers were identified by
All data were collected in triplicate and are expressed as the mean ± standard deviation. For the studies of the effect of food ingredients and catalysts on the thermal Z-isomerization of lycopene, Dunnett's test (p < 0.05 or p < 0.001) was used to evaluate statistical significance compared to the control group using JMP software (version 14.1.0; SAS Institute Inc., Cary, NC, USA). 3. Results and discussion 3.1. Profile of lycopene isomers obtained after thermal treatment Representative chromatograms of the untreated and thermally treated samples are shown in Fig. 1. Before heating, most of the 2
LWT - Food Science and Technology 116 (2019) 108565
M. Honda, et al.
seasoning (control), the total Z-isomer content increased to 32.3%. On the other hand, some seasonings significantly enhanced Z-isomerization. For example, when pickled caper and kneaded wasabi were added, the total Z-isomer content was found to be more than twice that of the control. The results indicated that caper (Capparis spinosa L.) and wasabi (Eutrema japonicum) enhanced thermal Z-isomerization. Thus, the presence of caper in tapenade is probably a major reason for the enhanced thermal Z-isomerization. Caper has traditionally been used in tomato dishes; however, this is the first report that caper enhances the thermal Z-isomerization of lycopene. Thermal Z-isomerization was notably promoted when jerk sauce, which is traditionally used in Jamaica, was added. The main constituent of this seasoning is escallion (Allium fistulosum L.), which is likely to be one of the causal food ingredients having a Z-isomerization promoting effect of (all-E)-lycopene. Several studies also reported that the food ingredients of Allium plants, such as onion and garlic, enhance the thermal Z-isomerization of lycopene (Rinaldi de Alvarenga et al., 2017; Honda et al., 2018b; Yu et al., 2019). Furthermore, seasonings that contain garlic as the main ingredient, such as black bean sauce, aioli, and gochujang (Table S1), promoted the thermal Z-isomerization of (all-E)-lycopene. These results indicate that most Allium plants can enhance this process. Dijon mustard, which contains mustard (Brassica juncea L.) as the main component, exhibited the Z-isomerization promoting effect. A few studies have also indicated that Brassica plants, such as broccoli and cabbage, promote thermal isomerization of (all-E)-lycopene (Honda et al., 2019; Takemura, Honda, & Fukaya, 2019). In addition, some fish sauces such as nuocmam and shottsuru, yeast extracts such as marmite and vegemite, and cooking liquors such as mirin and red wine enhanced thermal Z-isomerization. The relative proportion of the 5Z-isomer, which is characterized by high functionality and storage stability among the Z-isomers (Honda et al., 2018a; Müller et al., 2011; Murakami et al., 2018), is shown in Fig. 2B. The 5Z-isomer content following heating was generally consistent with an increased degree of the total Z-isomer content. Of the 35 seasonings investigated, the top five that promoted 5Z-isomerization of lycopene following heating were as follows: jerk sauce (18.3%) > pickled caper (16.6%) > kneaded wasabi (16.2%) > tapenade (12.4%) > black bean sauce (10.7%) (Supplementary Table S2). From the above results, some causative components that promote thermal Z-isomerization can be deduced. We recently reported that
lycopene content in the sample was detected to be in all-E-configuration (Fig. 1A), whereas the percentage of Z-isomers increased following heating at 80 °C for 1 h (Fig. 1B), as described in previous reports (Honda et al., 2017b and 2017c). The addition of some seasonings such as jerk sauce and Dijon mustard clearly enhanced the thermal Z-isomerization and substantially changed the lycopene isomer profile in comparison to the profile in the absence of seasonings (see details in section 3.2.) (Fig. 1C and D). (13Z)-Lycopene was mainly increased in the thermally treated sample without seasoning (Fig. 1B, Table S2). On the other hand, the 9Z- and 5Z-isomers were predominantly increased in the presence of certain seasonings (Fig. 1C and D, Table S2). Several studies have shown that, among lycopene isomers, (5Z)-lycopene is likely to have higher bioavailability and antioxidant activity than the other isomers (Honda et al., 2018a; Müller et al., 2011). Moreover, the 5Z-isomer has the highest storage stability of the mono-Z-isomers and its stability is similar to the all-E-isomer (Honda et al., 2017a; Murakami et al., 2018). Namely, (13Z)- and (9Z)-lycopene are isomerized to the all-E-isomer during storage under the influence of heat and light, whereas (5Z)-lycopene is stable against heat and light (Murakami et al., 2018). To expand product storage life is essential from an industrial viewpoint and thus, it is very important to clarify the seasoning(s) that can increase the 5Z-isomer. Since (5Z)-lycopene has the highest activation energy (Ea) from the all-E-isomer to the mono-Zisomers (Honda et al., 2017a), its production from the all-E-isomer requires significant thermal energy. However, the addition of several seasonings, such as jerk sauce, resulted in the 5Z-isomer being the predominant Z-isomer produced (Fig. 1 D). This suggests that such seasonings are likely to contain catalysts like iron(III) chloride and diallyl disulfide, which lower the activation energy (Ea) for the production of (5Z)-lycopene from the all-E-isomer (Honda et al., 2018b; Honda, Kawana, Takehara, & Inoue, 2015a; Yu et al., 2019). 3.2. Effect of seasonings on thermal Z-isomerization of tomato lycopene The impact of 35 commercially available global traditional seasonings (Table S1) on thermal Z-isomerization of (all-E)-lycopene contained in tomato puree was investigated. After heating at 80 °C for 1 h, lycopene was not decomposed to any significant extent. (Table S2). The total Z-isomer content of lycopene following heating is shown in Fig. 2A. When the thermal treatment was performed in the absence of
Table 1 Tentative identification of lycopene isomers using normal-phase high-performance liquid chromatography with diode array detector.a Peak
Lycopene isomerb
λmax (nm)
Q-Ratio
Observed 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
(9Z,13′Z) ULZ (9Z, 9′Z) ULZ ULZ (5Z,13′Z) (13Z) ULZ ULZ ULZ ULZ (5Z,9′Z) ULZ (9Z) (5Z,9Z,5′Z) (5Z,9Z) (5Z,5′Z) (all-E) (5Z)
360, 361, 360, 360, 360, 360, 360, 360, 360, 360, 360, 361, 360, 360, 360, 360, 442, 444, 444,
432, 432, 432, 440, 432, 440, 439, 441, 432, 432, 432, 439, 432, 439, 442, 438, 469, 470, 470,
Reported 458, 457, 461, 465, 457, 465, 464, 467, 457, 457, 457, 464, 452, 463, 463, 463, 502 501 501
488 484 488 496 484 497 496 498 484 484 484 495 487 495 496 495
361, – 361, – – 361, 361, – – – – 361, – 361, 361, 361, 443, 444, 444,
b
434, 459, 489 435, 460, 491
439, 465, 497 437, 463, 494
442, 467, 497 442, 442, 440, 470, 471, 471,
467, 497 467, 497 460, 497 501 502 502
Observed
Reportedb
0.29 0.24 0.11 0.42 0.25 0.43 0.44 0.32 23.7 0.11 0.24 0.13 0.26 0.14 0.12 0.12 ND ND ND
0.31 – 0.11 – – 0.56 0.59 – – – – 0.13 – 0.13 0.13 0.13 ND ND ND
a Values and peak designations were obtained from the chromatograms in Fig. 1. ULZ, unidentified lycopene Z-isomer. –, not assigned. ND, not detected substantially. b Tentatively assigned in the literatures (Hengartner, U., Bernhard, K., Meyer, K., Englert, G., & Glinz, 1992; Honda et al., 2015b and 2017a).
3
LWT - Food Science and Technology 116 (2019) 108565
M. Honda, et al.
Fig. 2. Effect of addition of seasonings on the thermal Z-isomerization of lycopene contained in tomato puree. (A) Effect on total Z-isomer content, (B) effect on 5Zisomer content. Error bars show standard deviation (n = 3). * and ** indicate statistically significant differences (Dunnett's test) from the control group at p < 0.05 and p < 0.001, respectively.
dissolved in ethanol (0.6 mg/L at 20 °C; Murakami et al., 2017). Our findings on the effect of the addition of seasonings on the thermal Zisomerization of lycopene are important, not only for the food and beverage manufacturing industries, but also for developing more nutritious home cooking recipes.
diallyl disulfide, which is frequently found in plants of the Allium species, enhanced thermal Z-isomerization of (all-E)-lycopene (Honda et al., 2018b). Thus, it is thought that polysulfides would be a causative component of the seasonings containing escallion (Allium fistulosum L.) and garlic (Allium sativum L.), e.g., jerk sauce and aioli. Moreover, disulfide compounds are produced by the Maillard reaction (Xu, Liu, Zhao, & Gao, 2008). Since the Maillard reaction occurs during the fermentation of fish sauce and yeast extract, the causative components of those seasonings are suggested to be the disulfide compounds. In fact, several studies have reported that fish sauce (nam-pla) and yeast extract contain diallyl disulphide (Lin et al., 2014; Yongsawatdigul, Rodtong, & Raksakulthai, 2007). This study revealed that caper, wasabi, and mustard might promote the Z-isomerization reaction. Our recent study shows that isothiocyanates promote the thermal Z-isomerization of (allE)-lycopene (Honda et al., 2019), and these food ingredients commonly contain considerable quantities of isothiocyanates such as allyl isothiocyanate and benzyl isothiocyanate (Jordt et al., 2004). Thus, it is proposed that the presence of isothiocyanates accounts for the ability of pickled caper, kneaded wasabi, tapenade, and Dijon mustard to promote the thermal Z-isomerization of (all-E)-lycopene. Cooking alcohols also promoted this process, with ethanol being one of the causative components. Several studies have reported that the presence of a mediator(s), i.e., organic solvents and oils, enhanced thermal Z-isomerization of (all-E)-carotenoids (Honda et al., 2015b and 2017b). Namely, E/Z-isomerization reaction of carotenoids is more facile in a dissolved state. Although the solubility is low, (all-E)-lycopene can be
4. Conclusions The effect of 35 global traditional seasonings on thermal Z-isomerization of (all-E)-lycopene contained in tomato puree was investigated. Several seasonings, e.g., jerk sauce, tapenade, aioli, and Dijon mustard, notably promoted the Z-isomerization. We attribute this to the presence of causal food ingredients such as escallion (Allium fistulosum L.), caper (Capparis spinosa L.), garlic (Allium sativum L.), and mustard (Brassica juncea L.), which contain disulfide compounds and isothiocyanates that lower the activation energy, and therefore, enhance the Z-isomerization process. These findings are important, not only for the production of high value-added processed tomato products, but also for optimal nutrition when cooking at home. Acknowledgements This work was partly supported by JSPS KAKENHI Grant Number 19K15779and the Tatematsu Foundation, and the Hokuto Foundation for Bioscience. The authors are grateful to T. Kumagai, C. Kitamura, Y. Inoue, and M. Takehara (The University of Shiga Prefecture), and H. 4
LWT - Food Science and Technology 116 (2019) 108565
M. Honda, et al.
Ueda, T. Higashiura, and R. Takemura (Kagome Co., Ltd.) for their kind help and constructive suggestions.
Microwave-accelerated Z-isomerization of (all-E)-lycopene in tomato oleoresin and enhancement of the conversion by vegetable oils containing disulfide compounds. European Journal of Lipid Science and Technology, 120(1–9), 1800060. Honda, M., Takahashi, N., Kuwa, T., Takehara, M., Inoue, Y., & Kumagai, T. (2015b). Spectral characterisation of Z-isomers of lycopene formed during heat treatment and solvent effects on the E/Z isomerisation process. Food Chemistry, 171, 323–329. Honda, M., Watanabe, Y., Murakami, K., Takemura, R., Fukaya, T., Kanda, H., et al. (2017c). Thermal isomerization pre-treatment to improve lycopene extraction from tomato pulp. LWT-Food Science and Technology, 86, 69–75. Jordt, S. E., Bautista, D. M., Chuang, H. H., McKemy, D. D., Zygmunt, P. M., Högestätt, E. D., et al. (2004). Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature, 427, 260–265. Lin, M., Liu, X., Xu, Q., Song, H., Li, P., & Yao, J. (2014). Aroma‐active components of yeast extract pastes with a basic and characteristic meaty flavour. Journal of the Science of Food and Agriculture, 94, 882–889. Murakami, K., Honda, M., Takemura, R., Fukaya, T., Kanda, H., & Goto, M. (2018). Effect of thermal treatment and light irradiation on the stability of lycopene with high Zisomers content. Food Chemistry, 250, 253–258. Murakami, K., Honda, M., Takemura, R., Fukaya, T., Kubota, M., Kanda, H., et al. (2017). The thermal Z-isomerization-induced change in solubility and physical properties of (all-E)-lycopene. Biochemical and Biophysical Research Communications, 491, 317–322. Müller, L., Goupy, P., Fröhlich, K., Dangles, O., Caris-Veyrat, C., & Böhm, V. (2011). Comparative study on antioxidant activity of lycopene (Z)-isomers in different assays. Journal of Agricultural and Food Chemistry, 59, 4504–4511. Perveen, R., Suleria, H. A. R., Anjum, F. M., Butt, M. S., Pasha, I., & Ahmad, S. (2015). Tomato (Solanum lycopersicum) carotenoids and lycopenes chemistry; metabolism, absorption, nutrition, and allied health claims—a comprehensive review. Critical Reviews in Food Science and Nutrition, 55, 919–929. Rinaldi de Alvarenga, J. F., Tran, C., Hurtado-Barroso, S., Martinez-Huélamo, M., Illan, M., & Lamuela-Raventos, R. M. (2017). Home cooking and ingredient synergism improve lycopene isomer production in Sofrito. Food Research International, 99, 851–861. Ryan, L., O'Connell, O., O'Sullivan, L., Aherne, S. A., & O'Brien, N. M. (2008). Micellarisation of carotenoids from raw and cooked vegetables. Plant Foods for Human Nutrition, 63, 127–133. Takemura, R., Honda, M., & Fukaya, T. (2019). Enhanced cis-isomerization of (all-trans)lycopene in tomato products with via specific vegetables in home cooking. Journal of Cookery Science of Japan, 52, 57–66. Xu, H., Liu, X., Zhao, J., & Gao, Y. (2008). Effects of ribose to cysteine ratios on the formation of volatile compounds from the Maillard reaction in supercritical carbon dioxide. Food Research International, 41, 730–737. Yongsawatdigul, J., Rodtong, S., & Raksakulthai, N. (2007). Acceleration of Thai fish sauce fermentation using proteinases and bacterial starter cultures. Journal of Food Science, 72, M382–M390. Yu, J., Gleize, B., Zhang, L., Caris-Veyrat, C., & Renard, C. M. (2019). Heating tomato puree in the presence of lipids and onion: The impact of onion on lycopene isomerization. Food Chemistry, 296, 9–16.
Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.lwt.2019.108565. References Capanoglu, E., Beekwilder, J., Boyacioglu, D., De Vos, R. C., & Hall, R. D. (2010). The effect of industrial food processing on potentially health-beneficial tomato antioxidants. Critical Reviews in Food Science and Nutrition, 50, 919–930. Cooperstone, J. L., Ralston, R. A., Riedl, K. M., Haufe, T. C., Schweiggert, R. M., King, S. A., et al. (2015). Enhanced bioavailability of lycopene when consumed as cis-isomers from tangerine compared to red tomato juice, a randomized, cross-over clinical trial. Molecular Nutrition & Food Research, 59, 658–669. Hengartner, U., Bernhard, K., Meyer, K., Englert, G., & Glinz, E. (1992). Synthesis, isolation, and NMR-spectroscopic characterization of fourteen (Z)-isomers of lycopene and of some acetylenic didehydro- and tetradehydrolycopenes. Helvetica Chimica Acta, 75, 1848–1865. Honda, M., Kageyama, H., Hibino, T., Takemura, R., Goto, M., & Fukaya, T. (2019a). Enhanced Z-isomerization of tomato lycopene through the optimal combination of food ingredients. Scientific Reports, 9(1–7), 7979. Honda, M., Kageyama, H., Hibino, T., Zhang, Y., Wahyudiono Kanda, H., et al. (2019b). Improved carotenoid processing with sustainable solvents utilizing Z-isomerizationinduced alteration in physicochemical properties: A review and future directions. Molecules, 24(1–19), 2149. Honda, M., Kawana, T., Takehara, M., & Inoue, Y. (2015a). Enhanced E/Z isomerization of (all-E)-lycopene by employing iron(III) chloride as a catalyst. Journal of Food Science, 80, C1453–C1459. Honda, M., Kudo, T., Kuwa, T., Higashiura, T., Fukaya, T., Inoue, Y., et al. (2017a). Isolation and spectral characterization of thermally generated multi-Z-isomers of lycopene and the theoretically preferred pathway to di-Z-isomers. Bioscience, Biotechnology, and Biochemistry, 81, 365–371. Honda, M., Maeda, H., Fukaya, T., & Goto, M. (2018a). Effects of Z-isomerization on the bioavailability and functionality of carotenoids: A review. In L. Q. Zepla, E. JacobLopes, & V. V. De Rosso (Eds.). Progress in carotenoid research (pp. 139–159). London: IntechOpen. Honda, M., Murakami, K., Watanabe, Y., Higashiura, T., Fukaya, T., Kanda, H., et al. (2017b). The E/Z isomer ratio of lycopene in foods and effect of heating with edible oils and fats on isomerization of (all-E)-lycopene. European Journal of Lipid Science and Technology, 119(1–9), 1600389. Honda, M., Sato, H., Takehara, M., Inoue, Y., Kitamura, C., Takemura, R., et al. (2018b).
5