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Assessing the supercooling of fresh-cut onions at −5°C using electrical impedance analysis

Assessing the supercooling of fresh-cut onions at −5°C using electrical impedance analysis We supercooled fresh-cut onion at −5°C for 12 h. After supercooling, the electric impedance properties of the samples were evaluated by electrical impedance spectroscopy over the frequency range of 42 Hz − 5 MHz. The time-temperature profiles of samples indicated that the freezing point and supercooling point were −2.3°C ± 0.7°C and −6.9°C ± 1.0°C, respectively. The results indicated that 34 of the 36 supercooled samples exhibited a definite circular arc in the Cole-Cole plot, which suggested that the cell membrane remained intact during supercooling. In the other two samples which did not exhibit a definite circular arc, the cell membrane had sustained serious damage during supercooling. Furthermore, there was large difference in drip loss percentage between supercooled samples exhibited a definite circular arc in the Cole-Cole plot and samples not exhibiting a definite circular arc. Our results suggest that fresh-cut onions can be supercooled at −5°C. Key words: supercooling; fresh-cut onion; electrical impedance; Cole-Cole plot; supercooling point. fresh-cut vegetables, except for experimental data on fresh-cut cab- Introduction bage (Koide et al., 2017), leaf lettuce (Quang et al., 2017), and fresh- The use of low temperature is a common preservation method world- cut spinach (Koide et al., 2019). In general, fresh-cut vegetables are wide for maintaining the freshness of vegetables and fruit because low highly susceptible to microbial spoilage, because of the slicing and temperatures reduce the microbial growth, biochemical reactions, res- peeling operations during their processing (Koseki and Itoh, 2001). piration, and transpiration of these products. The best temperature Thus, if the supercooling procedure could be applied to fresh-cut for slowing down deterioration is the lowest temperature that can vegetables, it would reduce the rate of degradation from microbial safely be maintained during preservation without freezing the prod- sources (spoilage and pathogenic), thereby increasing their shelf life ucts. Recently, new research into food refrigeration and storage tech- in the food cold chain. nologies has proposed alternative methods for extending the shelf life The present study investigated fresh-cut onions, a commonly used of fresh foods by using supercooling (Stonehouse and Evans, 2015), cut vegetable, for supercooling tests at a sub-zero temperature. Since although a supercooled food product is unstable because spontaneous our preliminary tests showed that most fresh-cut onions preserved nucleation can occur at any moment (Cox and Moore, 1997). at −5°C exhibited little drip loss and little colour deterioration but Previous studies have reported that some vegetables, such as significant drip losses and colour deterioration at around a tempera- garlic, shallots, and peppers, broccoli, and cauliflowers which have ture of −7°C after 12 h, we supercooled the fresh-cut onion at −5°C been cooled at a slow rate can be stored in a supercooled state at for 12 h. The aim of this study is to measure the freezing point and temperatures significantly below their freezing points without supercooling point of the sample, and to investigate the supercooled freezing occurring (James et al., 2009; James et al., 2011). However, sample using electrical impedance spectroscopy (EIS) to understand few studies are available on the application of supercooling to the status of the cell membrane of the fresh-cut onions. In addition, © The Author(s) 2020. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by- nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz044/5721965 by guest on 19 February 2020 2 Koide et al. the drip loss percentage of supercooled sample was investigated. To computer for analysis. The resistance, R (Ω), and reactance, X (Ω), our knowledge, this is the first study to assess the supercooling of were calculated using the following equations: fresh-cut vegetables using bulbs vegetables. R = |Z| cos θ Materials and Methods Materials X = |Z| sin θ Onion bulbs (Allium cepa) were purchased from August to October 2018, at a local supermarket in Morioka, Japan, then stored at room temperature in a dark incubator before the experiment. The experi- Statistical analysis ments on the onion bulbs were performed within a period of 7 days. The quantitative data are presented as means ± SD. The onion bulbs were cut longitudinally into 12 equal parts, then the outer and second leaves were removed. The third and fourth leaves Results and Discussion were separated by hand then weighed immediately and used as the sample for the supercooling tests. In the present study, samples just Temperature profile of sample during the cut from the onion bulbs were used as the control. Samples stored supercooling tests in a deep freezer at −80°C for 24 h, followed by thawing at room A representative temperature profile for a fresh sample used in the temperature (dead sample; DS) were used as negative controls. The supercooling test is shown in Figure  1. The sample was cooled at average mass of the sample was 2.90 ± 0.08 g with an average mois- 0.5°C/min from 0°C to −2°C. In these measurements, no samples ture content of 93.7% ± 0.1% (wet basis), determined using the oven with a thermocouple positioned in the tissue exhibited an exotherm drying method (105°C for 24 h). in their temperature profiles under supercooling, thereby indicating that the samples were in a supercooled state. Supercooling test Each sample was placed in a 50-ml test tube (2344-050; Iwaki, Freezing point and supercooling point Sekiyarika Co. Ltd, Tokyo, Japan) then covered with a tube cap for A representative time-temperature profile for a fresh-cut onion the supercooling test. A  refrigerated liquid circulating bath (NCB- sample for measuring the freezing point and supercooling point is 3300; Eyela, Tokyo Rikakikai Co. Ltd., Tokyo, Japan) was used for shown in Figure  2. The freezing point of the fresh samples deter- this test. The measurements were made while the test tubes were sub- mined from the time-temperature profiles averaged −2.3°C ± 0.7°C, merged in ethanol at −5°C. A T-type thermocouple positioned at the similar to those reported for other vegetables: broccoli (−2.1°C ± geometric centre of the sample was used to measure the temperature. 0.3°C), carrots (−1.6°C ± 0.6°C), and shallots (−1.6°C ± 0.2°C) The samples were then stored at −5°C for 12 h. After supercooling, (James et  al., 2011), fresh-cut swede (−2.65°C ± 0.35°C) and the samples were warmed to 10°C for 12 h then brought to room fresh-cut turnip (−1.97°C ± 0.51°C) (Helland et  al., 2016). Next, temperature at 25°C. The samples, except for those used for tem- the supercooling points were obtained in the range from −5.3°C to perature measurement using a thermocouple, were measured using −8.2°C, with a mean value of −6.9°C ± 1.0°C, which was lower than EIS. The experiments were repeated four times. those reported for other vegetables: broccoli (−4.4°C ± 2.4°C), car- rots (−2.7°C ± 0.8°C), and shallots (−5.4°C ± 1.4°C) (James et  al., Supercooling point and freezing point 2011), but similar to those of fresh-cut swede (−6.26°C ± 2.45°C), The time-temperature profiles of the samples (n = 9) were also meas- and fresh-cut turnip (−6.37°C ± 1.59°C) (Helland et al., 2016). The ured to determine the freezing point of the fresh samples. This ex- present results demonstrate that fresh-cut onion can be preserved at periment was performed in the same way as the supercooling test a temperature of −5°C. However, more information on the effects but with the following modification. A sample of tissue with a T-type thermocouple positioned at its geometric centre was placed in a 50-ml test tube then cooled to −5°C in the refrigerated liquid cir- culating bath. When the sample temperature reached −5°C, it was cooled further to −15°C at approximately 0.2°C/min by reducing the temperature of the ethanol in the refrigerated circulating bath. The temperature when the low temperature exothermic occurred in the time-temperature profile was taken as the supercooling point. The freezing point was indicated by the plateau in the time-temperature profiles where the measured temperature is almost constant after rising from that for the supercooled state (Meng et al., 2007). Electrical impedance measurement The electrical impedance data from the supercooled, control, and DS samples were measured by EIS as described by Wu et al. (2008). The impedance of each sample was measured using two parallel electrodes spaced 10 mm apart (3532–50, Hioki Corp. E.E., Ueda, Japan). The impedance magnitude, |Z|, and phase angle, θ, of the samples were measured at 50 frequency points (logarithmic fre- quency intervals) over the frequency range of 42 Hz–5 MHz under Figure 1. A representative temperature profile of a fresh-cut onion sample a measuring voltage of 1.0 V, and automatically recorded by a supercooled at −5°C for 12 h then warmed to 10°C for 12 h. °C Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz044/5721965 by guest on 19 February 2020 Supercooling of fresh-cut onions 3 Figure 3. Impedance of fresh-cut onion samples supercooled at −5°C. Open circles represent F (fresh sample), times symbols represent DS (frozen- Figure 2. A representative time-temperature profile of a fresh-cut onion thawed sample), open diamonds represent SC-1 (supercooled sample with sample indicating its freezing and supercooling points. The solid line a high impedance at 1  kHz, the same as that of the fresh sample; applied represents the temperature-profile of the sample, and the dashed line that of to 34/36 samples), and closed diamonds represent SC-2 (supercooled the ethanol in the refrigerated circulating bath. sample with a low impedance at 1  kHz, the same as that of DS; applied to 2/36 samples). Each value represents the mean (SD). Measurements were of speed of cooling, sample size, preservation time in relation to ice performed in quadruplicate. formation are needed for future investigations. Electrical impedance EIS is often used to analyse the physical state of cell membranes in biological tissues (Zhang and Willison, 1992; Wu et al., 2008; Ando et  al., 2016; Watanabe et  al., 2016). The structural properties of the cell appear in the range of frequencies from approximately 100 Hz to 10 MHz (Ando et al., 2014). The impedance of the fresh-cut onion as the control, the supercooled sample, and DS as the negative control were plotted with respect to frequency (Figure 3). Focusing on the control, there was a clear dependence of the impedance on frequency: the impedance decreased as the frequency increased, es- pecially between 1 and 100  kHz. This dependence of impedance on frequency showed that the cell tissue structure was composed of an aggregation of closed cell spaces separated by cell membrane (Ohnishi et  al., 2003). While the impedance of DS at a lower fre- quency was very low compared with the control, it was almost inde- pendent of the frequency between 1 kHz and 5 MHz, showing that the cell membrane had been so seriously damaged that it could no Figure 4. Cole-Cole plots of the fresh-cut onion samples supercooled at −5°C. longer retain the cell contents (Wu et al., 2008). The Cole-Cole plots Open circles represent F (fresh sample), times symbols represent DS (frozen- for the control, supercooled, and DS samples are shown in Figure 4. thawed sample), open diamonds represent SC-1 (supercooled sample with The right side of the circular arc describes a low frequency area, a high impedance at 1 kHz, the same as that of the fresh sample; applied to and the left side a high frequency area. It has been reported that 34/36 samples), and closed diamonds represent SC-2 (supercooled sample the Cole-Cole plot for fresh vegetables describes a circular arc (Wu with a low impedance at 1  kHz, the same as that of DS; applied to 2/36 et al., 2008; Watanabe et al., 2016), but no arcs were produced for samples). Each value represents the mean. Measurements were performed in quadruplicate. the frozen-thawed samples. Similar results have been reported for several frozen-thawed vegetables: carrots (Ohnishi et al., 2003), egg- plant (Wu et  al., 2008), potato (Ohnishi et  al., 2003; Ando 2014), supercooled samples with a low impedance at 1  kHz) had a very fresh-cut cabbage (Koide et al., 2017), and fresh-cut spinach (Koide low impedance similar to that for DS (Figure 3), and there were no et al., 2019). definite circular arcs in the Cole-Cole plots (Figure  4), almost the Regarding the supercooled samples, the impedance of 34 of the same trend as for DS. 36 samples (SC-1: supercooled samples with a high impedance at The average values of drip losses, expressed as the loss of weight 1 kHz, the same as that for the fresh sample) depended on frequency of the sample after supercooling as a percentage of the initial weight, (Figure  3), and there were definite circular arcs in the Cole-Cole were 2.0% for SC-1 and 13.6% for SC-2. While, the average drip plots (Figure  4), suggesting that the cell membranes had remained loss percentage of DS was 18.6%. The large difference in drip loss intact after supercooling. However, 2 of the 36 samples (SC-2: percentage between SC-1 and SC-2 may be due to the state of cell °C Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz044/5721965 by guest on 19 February 2020 4 Koide et al. roots in relation to changes in cell membrane function and cell wall struc- membranes before and after supercooling. Taking the results of EIS, ture. LWT - Food Science and Technology, 71: 40–46. it can be suggested that the physiological structure of the cell mem- Ando,  Y., Mizutani,  K., Wakatsuki,  N. (2014). Electrical impedance ana- branes of SC-2 had been disrupted by the ice crystals formed during lysis of potato tissues during drying. Journal of Food Engineering, 121: the supercooled state of the test sample. 24–31. The temperature profile of the sample during supercooling and the Cox, D., Moore, S. (1997). A Process for Supercooling. Patent Application No. evaluation of the supercooled sample by EIS indicated that fresh-cut WO97/18879. World Intellectual Property Organisation. onions could be preserved by supercooling at −5°C. This would con- Helland,  H.  S., Leufvén,  A., Bengtsson,  G.  B., Pettersen,  M.  K., Lea,  P., tribute to reducing the amount of product wastage and the negative Wold, A. B. (2016). Storage of fresh-cut swede and turnip: effect of tem- indices of marketability such as drip loss, visual alterations, and colour perature, including sub-zero temperature, and packaging material on sen- deterioration (Ohnishi et al., 2003; Stonehouse and Evans, 2015; Jha sory attributes, sugars and glucosinolates. Postharvest Biology and Tech- nology, 111: 370–379. et al., 2019). Further investigations into the supercooling preservation James, C., Hanser, P., James, S. J. (2011). Super-cooling phenomena in fruits, of fresh-cut vegetables regarding temperatures and durations of treat- vegetables and seafoods. In: Proceedings of 11th International Congress ment to achieve stable supercooling conditions are underway. on Engineering and Food (ICEF 2011), Athens, Greece, pp. 22–26. James, C., Seignemartin, V., James, S. J. (2009). The freezing and supercooling of garlic (Allium sativum L.). International Journal of Refrigeration, 32: Conclusions 253–260. In this study, fresh-cut onions were preserved by supercooling at Jha, P. K., Xanthakis, E., Chevallier, S., Jury, V., Le-Bail, A. (2019). Assessment −5°C for 12 h, with the following conclusions: of freeze damage in fruits and vegetables. Food Research International (Ottawa, Ont.), 121: 479–496. Koide, S., Kumada, R., Hayakawa, K., Kawakami, I., Orikasa, T., Katahira, M., (1) The time-temperature profiles of the samples indicated that the Uemura, M. (2017). Survival of cut cabbage subjected to subzero temper- freezing and supercooling point were −2.3°C ± 0.7°C and −6.9°C atures. In: Proceedings of VI Postharvest Unlimited: ISIH International ± 1.0°C, respectively. Conference, 17–20 October 2017, Madrid, Spain. http://postharvest2017. (2) The dependence of impedance on frequency leading to the Cole- sicongresos.com/posters/23.jpg. Accessed 6 November 2019. Cole plots would be an effective method for assessing the super- Koide, S., Ohsuga, R., Orikasa, T., Uemura, M. (2019). Evaluation of electrical cooling of fresh-cut onions. and physiological properties of supercooled fresh cut spinach. Journal of (3) Electrical impedance spectroscopy (EIS) indicated that the cell the Japanese Society for Food Science and Technology - Nippon Shokuhin membranes of most of the supercooled samples remained intact. Kagaku Kogaku Kaishi, 66: 335–340. (In Japanese with English abstract). Koseki, S., Itoh, K. (2001). Prediction of microbial growth in fresh-cut veget- Our study suggests that fresh-cut onions can be supercooled at −5°C. ables treated with acidic electrolyzed water during storage under various temperature conditions. Journal of Food Protection, 64: 1935–1942. Meng, Q. R., Liang, Y. Q., Wang, W. F., Du, S. H., Li, Y. H., Yang, J. M. (2007). Funding Study on supercooling point and freezing point in floral organs of apricot. This work was supported by JSPS KAKENHI, grant number JP16H05001 Agricultural Sciences in China, 6: 1330–1335. [Grant-in-Aid for Scientific Research (B)] and JP16K15010 [Grant-in-Aid Ohnishi,  S., Fujii,  T., Miyawaki,  O. (2003). Freezing injury and rheological for Exploratory Research]. properties of agricultural products. Food Science and Technology Re- search, 9: 367–371. Quang,  T.  N., Iwamura,  K., Shrestha,  R., Sugimura,  N. (2017). A study on supercooled storage of leaf lettuces produced in plant factory. Japan Author contributions Journal of Food Engineering, 18: 25–32. SK coordinates the study, AY contributed to the measurement and analysis of Stonehouse,  G.  G., Evans,  J.  A. (2015). The use of supercooling for fresh all data, TU contributed to the discussion of the electrical impedance analysis, foods: a review. Journal of Food Engineering, 148: 74–79. and MU contributed to the discussion of supercooling state from viewpoints Watanabe,  T., Orikasa,  T., Shono,  H., Koide,  S., Ando,  Y., Shiina,  T., of cryobiology. Tagawa, A. (2016). The influence of inhibit avoid water defect responses by heat pretreatment on hot air drying rate of spinach. Journal of Food Engineering, 168: 113–118. Conflict of Interest Statement Wu,  L., Ogawa,  Y., Tagawa,  A. (2008). Electrical impedance spectroscopy None declared. analysis of eggplant pulp and effects of drying and freezing-thawing treat- ments on its impedance characteristics. Journal of Food Engineering, 87: 274–280. References Zhang, M. I. N., Willison, J. H. M. (1992). Electrical impedance analysis in Ando,  Y., Maeda,  Y., Mizutani,  K., Hagiwara,  S.  W., Nabetani,  H. (2016). plant tissues: the effect of freeze-thaw injury on the electrical properties of Impact of blanching and freeze-thaw pretreatment on drying rate of carrot potato. Canadian Journal of Plant Science, 72: 545–553. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Food Quality and Safety Oxford University Press

Assessing the supercooling of fresh-cut onions at −5°C using electrical impedance analysis

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Abstract

We supercooled fresh-cut onion at −5°C for 12 h. After supercooling, the electric impedance properties of the samples were evaluated by electrical impedance spectroscopy over the frequency range of 42 Hz − 5 MHz. The time-temperature profiles of samples indicated that the freezing point and supercooling point were −2.3°C ± 0.7°C and −6.9°C ± 1.0°C, respectively. The results indicated that 34 of the 36 supercooled samples exhibited a definite circular arc in the Cole-Cole plot, which suggested that the cell membrane remained intact during supercooling. In the other two samples which did not exhibit a definite circular arc, the cell membrane had sustained serious damage during supercooling. Furthermore, there was large difference in drip loss percentage between supercooled samples exhibited a definite circular arc in the Cole-Cole plot and samples not exhibiting a definite circular arc. Our results suggest that fresh-cut onions can be supercooled at −5°C. Key words: supercooling; fresh-cut onion; electrical impedance; Cole-Cole plot; supercooling point. fresh-cut vegetables, except for experimental data on fresh-cut cab- Introduction bage (Koide et al., 2017), leaf lettuce (Quang et al., 2017), and fresh- The use of low temperature is a common preservation method world- cut spinach (Koide et al., 2019). In general, fresh-cut vegetables are wide for maintaining the freshness of vegetables and fruit because low highly susceptible to microbial spoilage, because of the slicing and temperatures reduce the microbial growth, biochemical reactions, res- peeling operations during their processing (Koseki and Itoh, 2001). piration, and transpiration of these products. The best temperature Thus, if the supercooling procedure could be applied to fresh-cut for slowing down deterioration is the lowest temperature that can vegetables, it would reduce the rate of degradation from microbial safely be maintained during preservation without freezing the prod- sources (spoilage and pathogenic), thereby increasing their shelf life ucts. Recently, new research into food refrigeration and storage tech- in the food cold chain. nologies has proposed alternative methods for extending the shelf life The present study investigated fresh-cut onions, a commonly used of fresh foods by using supercooling (Stonehouse and Evans, 2015), cut vegetable, for supercooling tests at a sub-zero temperature. Since although a supercooled food product is unstable because spontaneous our preliminary tests showed that most fresh-cut onions preserved nucleation can occur at any moment (Cox and Moore, 1997). at −5°C exhibited little drip loss and little colour deterioration but Previous studies have reported that some vegetables, such as significant drip losses and colour deterioration at around a tempera- garlic, shallots, and peppers, broccoli, and cauliflowers which have ture of −7°C after 12 h, we supercooled the fresh-cut onion at −5°C been cooled at a slow rate can be stored in a supercooled state at for 12 h. The aim of this study is to measure the freezing point and temperatures significantly below their freezing points without supercooling point of the sample, and to investigate the supercooled freezing occurring (James et al., 2009; James et al., 2011). However, sample using electrical impedance spectroscopy (EIS) to understand few studies are available on the application of supercooling to the status of the cell membrane of the fresh-cut onions. In addition, © The Author(s) 2020. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by- nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz044/5721965 by guest on 19 February 2020 2 Koide et al. the drip loss percentage of supercooled sample was investigated. To computer for analysis. The resistance, R (Ω), and reactance, X (Ω), our knowledge, this is the first study to assess the supercooling of were calculated using the following equations: fresh-cut vegetables using bulbs vegetables. R = |Z| cos θ Materials and Methods Materials X = |Z| sin θ Onion bulbs (Allium cepa) were purchased from August to October 2018, at a local supermarket in Morioka, Japan, then stored at room temperature in a dark incubator before the experiment. The experi- Statistical analysis ments on the onion bulbs were performed within a period of 7 days. The quantitative data are presented as means ± SD. The onion bulbs were cut longitudinally into 12 equal parts, then the outer and second leaves were removed. The third and fourth leaves Results and Discussion were separated by hand then weighed immediately and used as the sample for the supercooling tests. In the present study, samples just Temperature profile of sample during the cut from the onion bulbs were used as the control. Samples stored supercooling tests in a deep freezer at −80°C for 24 h, followed by thawing at room A representative temperature profile for a fresh sample used in the temperature (dead sample; DS) were used as negative controls. The supercooling test is shown in Figure  1. The sample was cooled at average mass of the sample was 2.90 ± 0.08 g with an average mois- 0.5°C/min from 0°C to −2°C. In these measurements, no samples ture content of 93.7% ± 0.1% (wet basis), determined using the oven with a thermocouple positioned in the tissue exhibited an exotherm drying method (105°C for 24 h). in their temperature profiles under supercooling, thereby indicating that the samples were in a supercooled state. Supercooling test Each sample was placed in a 50-ml test tube (2344-050; Iwaki, Freezing point and supercooling point Sekiyarika Co. Ltd, Tokyo, Japan) then covered with a tube cap for A representative time-temperature profile for a fresh-cut onion the supercooling test. A  refrigerated liquid circulating bath (NCB- sample for measuring the freezing point and supercooling point is 3300; Eyela, Tokyo Rikakikai Co. Ltd., Tokyo, Japan) was used for shown in Figure  2. The freezing point of the fresh samples deter- this test. The measurements were made while the test tubes were sub- mined from the time-temperature profiles averaged −2.3°C ± 0.7°C, merged in ethanol at −5°C. A T-type thermocouple positioned at the similar to those reported for other vegetables: broccoli (−2.1°C ± geometric centre of the sample was used to measure the temperature. 0.3°C), carrots (−1.6°C ± 0.6°C), and shallots (−1.6°C ± 0.2°C) The samples were then stored at −5°C for 12 h. After supercooling, (James et  al., 2011), fresh-cut swede (−2.65°C ± 0.35°C) and the samples were warmed to 10°C for 12 h then brought to room fresh-cut turnip (−1.97°C ± 0.51°C) (Helland et  al., 2016). Next, temperature at 25°C. The samples, except for those used for tem- the supercooling points were obtained in the range from −5.3°C to perature measurement using a thermocouple, were measured using −8.2°C, with a mean value of −6.9°C ± 1.0°C, which was lower than EIS. The experiments were repeated four times. those reported for other vegetables: broccoli (−4.4°C ± 2.4°C), car- rots (−2.7°C ± 0.8°C), and shallots (−5.4°C ± 1.4°C) (James et  al., Supercooling point and freezing point 2011), but similar to those of fresh-cut swede (−6.26°C ± 2.45°C), The time-temperature profiles of the samples (n = 9) were also meas- and fresh-cut turnip (−6.37°C ± 1.59°C) (Helland et al., 2016). The ured to determine the freezing point of the fresh samples. This ex- present results demonstrate that fresh-cut onion can be preserved at periment was performed in the same way as the supercooling test a temperature of −5°C. However, more information on the effects but with the following modification. A sample of tissue with a T-type thermocouple positioned at its geometric centre was placed in a 50-ml test tube then cooled to −5°C in the refrigerated liquid cir- culating bath. When the sample temperature reached −5°C, it was cooled further to −15°C at approximately 0.2°C/min by reducing the temperature of the ethanol in the refrigerated circulating bath. The temperature when the low temperature exothermic occurred in the time-temperature profile was taken as the supercooling point. The freezing point was indicated by the plateau in the time-temperature profiles where the measured temperature is almost constant after rising from that for the supercooled state (Meng et al., 2007). Electrical impedance measurement The electrical impedance data from the supercooled, control, and DS samples were measured by EIS as described by Wu et al. (2008). The impedance of each sample was measured using two parallel electrodes spaced 10 mm apart (3532–50, Hioki Corp. E.E., Ueda, Japan). The impedance magnitude, |Z|, and phase angle, θ, of the samples were measured at 50 frequency points (logarithmic fre- quency intervals) over the frequency range of 42 Hz–5 MHz under Figure 1. A representative temperature profile of a fresh-cut onion sample a measuring voltage of 1.0 V, and automatically recorded by a supercooled at −5°C for 12 h then warmed to 10°C for 12 h. °C Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz044/5721965 by guest on 19 February 2020 Supercooling of fresh-cut onions 3 Figure 3. Impedance of fresh-cut onion samples supercooled at −5°C. Open circles represent F (fresh sample), times symbols represent DS (frozen- Figure 2. A representative time-temperature profile of a fresh-cut onion thawed sample), open diamonds represent SC-1 (supercooled sample with sample indicating its freezing and supercooling points. The solid line a high impedance at 1  kHz, the same as that of the fresh sample; applied represents the temperature-profile of the sample, and the dashed line that of to 34/36 samples), and closed diamonds represent SC-2 (supercooled the ethanol in the refrigerated circulating bath. sample with a low impedance at 1  kHz, the same as that of DS; applied to 2/36 samples). Each value represents the mean (SD). Measurements were of speed of cooling, sample size, preservation time in relation to ice performed in quadruplicate. formation are needed for future investigations. Electrical impedance EIS is often used to analyse the physical state of cell membranes in biological tissues (Zhang and Willison, 1992; Wu et al., 2008; Ando et  al., 2016; Watanabe et  al., 2016). The structural properties of the cell appear in the range of frequencies from approximately 100 Hz to 10 MHz (Ando et al., 2014). The impedance of the fresh-cut onion as the control, the supercooled sample, and DS as the negative control were plotted with respect to frequency (Figure 3). Focusing on the control, there was a clear dependence of the impedance on frequency: the impedance decreased as the frequency increased, es- pecially between 1 and 100  kHz. This dependence of impedance on frequency showed that the cell tissue structure was composed of an aggregation of closed cell spaces separated by cell membrane (Ohnishi et  al., 2003). While the impedance of DS at a lower fre- quency was very low compared with the control, it was almost inde- pendent of the frequency between 1 kHz and 5 MHz, showing that the cell membrane had been so seriously damaged that it could no Figure 4. Cole-Cole plots of the fresh-cut onion samples supercooled at −5°C. longer retain the cell contents (Wu et al., 2008). The Cole-Cole plots Open circles represent F (fresh sample), times symbols represent DS (frozen- for the control, supercooled, and DS samples are shown in Figure 4. thawed sample), open diamonds represent SC-1 (supercooled sample with The right side of the circular arc describes a low frequency area, a high impedance at 1 kHz, the same as that of the fresh sample; applied to and the left side a high frequency area. It has been reported that 34/36 samples), and closed diamonds represent SC-2 (supercooled sample the Cole-Cole plot for fresh vegetables describes a circular arc (Wu with a low impedance at 1  kHz, the same as that of DS; applied to 2/36 et al., 2008; Watanabe et al., 2016), but no arcs were produced for samples). Each value represents the mean. Measurements were performed in quadruplicate. the frozen-thawed samples. Similar results have been reported for several frozen-thawed vegetables: carrots (Ohnishi et al., 2003), egg- plant (Wu et  al., 2008), potato (Ohnishi et  al., 2003; Ando 2014), supercooled samples with a low impedance at 1  kHz) had a very fresh-cut cabbage (Koide et al., 2017), and fresh-cut spinach (Koide low impedance similar to that for DS (Figure 3), and there were no et al., 2019). definite circular arcs in the Cole-Cole plots (Figure  4), almost the Regarding the supercooled samples, the impedance of 34 of the same trend as for DS. 36 samples (SC-1: supercooled samples with a high impedance at The average values of drip losses, expressed as the loss of weight 1 kHz, the same as that for the fresh sample) depended on frequency of the sample after supercooling as a percentage of the initial weight, (Figure  3), and there were definite circular arcs in the Cole-Cole were 2.0% for SC-1 and 13.6% for SC-2. While, the average drip plots (Figure  4), suggesting that the cell membranes had remained loss percentage of DS was 18.6%. The large difference in drip loss intact after supercooling. However, 2 of the 36 samples (SC-2: percentage between SC-1 and SC-2 may be due to the state of cell °C Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz044/5721965 by guest on 19 February 2020 4 Koide et al. roots in relation to changes in cell membrane function and cell wall struc- membranes before and after supercooling. Taking the results of EIS, ture. LWT - Food Science and Technology, 71: 40–46. it can be suggested that the physiological structure of the cell mem- Ando,  Y., Mizutani,  K., Wakatsuki,  N. (2014). Electrical impedance ana- branes of SC-2 had been disrupted by the ice crystals formed during lysis of potato tissues during drying. Journal of Food Engineering, 121: the supercooled state of the test sample. 24–31. The temperature profile of the sample during supercooling and the Cox, D., Moore, S. (1997). A Process for Supercooling. Patent Application No. evaluation of the supercooled sample by EIS indicated that fresh-cut WO97/18879. World Intellectual Property Organisation. onions could be preserved by supercooling at −5°C. This would con- Helland,  H.  S., Leufvén,  A., Bengtsson,  G.  B., Pettersen,  M.  K., Lea,  P., tribute to reducing the amount of product wastage and the negative Wold, A. B. (2016). Storage of fresh-cut swede and turnip: effect of tem- indices of marketability such as drip loss, visual alterations, and colour perature, including sub-zero temperature, and packaging material on sen- deterioration (Ohnishi et al., 2003; Stonehouse and Evans, 2015; Jha sory attributes, sugars and glucosinolates. Postharvest Biology and Tech- nology, 111: 370–379. et al., 2019). Further investigations into the supercooling preservation James, C., Hanser, P., James, S. J. (2011). Super-cooling phenomena in fruits, of fresh-cut vegetables regarding temperatures and durations of treat- vegetables and seafoods. In: Proceedings of 11th International Congress ment to achieve stable supercooling conditions are underway. on Engineering and Food (ICEF 2011), Athens, Greece, pp. 22–26. James, C., Seignemartin, V., James, S. J. (2009). The freezing and supercooling of garlic (Allium sativum L.). International Journal of Refrigeration, 32: Conclusions 253–260. In this study, fresh-cut onions were preserved by supercooling at Jha, P. K., Xanthakis, E., Chevallier, S., Jury, V., Le-Bail, A. (2019). Assessment −5°C for 12 h, with the following conclusions: of freeze damage in fruits and vegetables. Food Research International (Ottawa, Ont.), 121: 479–496. Koide, S., Kumada, R., Hayakawa, K., Kawakami, I., Orikasa, T., Katahira, M., (1) The time-temperature profiles of the samples indicated that the Uemura, M. (2017). Survival of cut cabbage subjected to subzero temper- freezing and supercooling point were −2.3°C ± 0.7°C and −6.9°C atures. In: Proceedings of VI Postharvest Unlimited: ISIH International ± 1.0°C, respectively. Conference, 17–20 October 2017, Madrid, Spain. http://postharvest2017. (2) The dependence of impedance on frequency leading to the Cole- sicongresos.com/posters/23.jpg. Accessed 6 November 2019. Cole plots would be an effective method for assessing the super- Koide, S., Ohsuga, R., Orikasa, T., Uemura, M. (2019). Evaluation of electrical cooling of fresh-cut onions. and physiological properties of supercooled fresh cut spinach. Journal of (3) Electrical impedance spectroscopy (EIS) indicated that the cell the Japanese Society for Food Science and Technology - Nippon Shokuhin membranes of most of the supercooled samples remained intact. Kagaku Kogaku Kaishi, 66: 335–340. (In Japanese with English abstract). Koseki, S., Itoh, K. (2001). Prediction of microbial growth in fresh-cut veget- Our study suggests that fresh-cut onions can be supercooled at −5°C. ables treated with acidic electrolyzed water during storage under various temperature conditions. Journal of Food Protection, 64: 1935–1942. Meng, Q. R., Liang, Y. Q., Wang, W. F., Du, S. H., Li, Y. H., Yang, J. M. (2007). Funding Study on supercooling point and freezing point in floral organs of apricot. This work was supported by JSPS KAKENHI, grant number JP16H05001 Agricultural Sciences in China, 6: 1330–1335. [Grant-in-Aid for Scientific Research (B)] and JP16K15010 [Grant-in-Aid Ohnishi,  S., Fujii,  T., Miyawaki,  O. (2003). Freezing injury and rheological for Exploratory Research]. properties of agricultural products. Food Science and Technology Re- search, 9: 367–371. Quang,  T.  N., Iwamura,  K., Shrestha,  R., Sugimura,  N. (2017). A study on supercooled storage of leaf lettuces produced in plant factory. Japan Author contributions Journal of Food Engineering, 18: 25–32. SK coordinates the study, AY contributed to the measurement and analysis of Stonehouse,  G.  G., Evans,  J.  A. (2015). The use of supercooling for fresh all data, TU contributed to the discussion of the electrical impedance analysis, foods: a review. Journal of Food Engineering, 148: 74–79. and MU contributed to the discussion of supercooling state from viewpoints Watanabe,  T., Orikasa,  T., Shono,  H., Koide,  S., Ando,  Y., Shiina,  T., of cryobiology. Tagawa, A. (2016). The influence of inhibit avoid water defect responses by heat pretreatment on hot air drying rate of spinach. Journal of Food Engineering, 168: 113–118. Conflict of Interest Statement Wu,  L., Ogawa,  Y., Tagawa,  A. (2008). Electrical impedance spectroscopy None declared. analysis of eggplant pulp and effects of drying and freezing-thawing treat- ments on its impedance characteristics. Journal of Food Engineering, 87: 274–280. References Zhang, M. I. N., Willison, J. H. M. (1992). Electrical impedance analysis in Ando,  Y., Maeda,  Y., Mizutani,  K., Hagiwara,  S.  W., Nabetani,  H. (2016). plant tissues: the effect of freeze-thaw injury on the electrical properties of Impact of blanching and freeze-thaw pretreatment on drying rate of carrot potato. Canadian Journal of Plant Science, 72: 545–553.

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Food Quality and SafetyOxford University Press

Published: Jul 17, 2020

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